Abstract
An increasing number of microorganisms are being identified as pathogens for diseases in macroalgae, but the species composition of bacteria related to Caulerpa lentillifera, fresh edible green macroalgae worldwide, remains largely unclear. The bacterial communities associated with C. lentillifera were investigated by high-throughput 16S rDNA sequencing, and the bacterial diversities in washed and control groups were compared in this study. A total of 4,388 operational taxonomic units were obtained from all the samples, and the predominant prokaryotic phyla were Proteobacteria, Bacteroidetes, Planctomycetes, Cyanobacteria, Actinobacteria, Verrucomicrobia, Chloroflexi, and Acidobacteria in C. lentillifera. The bacterial diversity changed with seasons and showed an increasing trend of diversity with the rising temperature in C. lentillifera. There were slight reductions in the abundance and diversity of bacteria after washing with tap water for 2 h, indicating that only parts of the bacterial groups could be washed out, and hidden dangers in C. lentillifera still exist. Although the reduction in the abundance of some bacteria revealed a positive significance of washing C. lentillifera with tap water on food safety, more effective cleaning methods still need to be explored.
1 Introduction
The genus Caulerpa (Bryopsidales, Chlorophyta), a siphonous green macroalgae, is widely distributed in subtropics and tropics, such as China, Singapore, Indonesia, the Philippines, Malaysia, Vietnam, and Japan. Some species of the genus are consumed as vegetables blended with onion, vinegar, or tomatoes [1]. For example, Indonesian Caulerpa usually is served as a side dish in South Sulawesi [2] and is used in fresh salads in Japan and many Asian regions [3]. C. lentillifera (sea grape), one of the most popular edible green macroalgae [1], which looks like grapes and is thus called green caviar [4,5,6].
The algae of genus Caulerpa are high in several vitamins and minerals, including iron, calcium, magnesium, and iodine [7,8,9]. Moreover, C. lentillifera contains a high level of polyunsaturated fatty acids and multiple essential amino acids (EAA) with low-level total lipid content [10]. The EAA composition of C. lentillifera approaches the ideal model recommended by the Food and Agriculture Organization/World Health Organization [11], and the reported protein content varies from 3.6 to 19.4% dry weight mass of C. lentillifera [6,12,13]. C. lentillifera also has potential functions, such as antidiabetic activity [14,15], anti-inflammatory activity [16], immunostimulatory activity [17], preventing hypertension [18], as well as anticoagulant and anticancer activity [19]. In recent years, C. lentillifera was introduced into China for a large-scale artificial cultivation as functional seafood. C. lentillifera was cultured with sand-filtered seawater on a double-layer net, under which a layer of sand was laid as an attachment base for rhizomes. The artificially cultivated C. lentillifera were raised in muddy ponds following standard culture conditions (20.0–32.0°C, 5,000–10,000 Lux) and were harvested regularly.
Diseases caused by seafood pose a critical hazard to public health worldwide [20]. The global consumption of seafood per capita has increased over the last few years [21]. The import and domestic aquaculture of seafood have also increased. Besides, some recent human gastroenteritis outbreaks have been associated with contaminated seafood consumption [22]. More details on pathogen virulence and pathogenicity should be obtained to investigate the seafood-borne disease caused by pathogens such as norovirus and Vibrio [3]. There are many foodborne pathogens in the marine environments, which may attach to the surface of seafood and enter the human body on consumption in fresh and live forms, thereby leading to several health risks. For example, Vibrio parahaemolyticus is a facultative, anaerobic, gram-negative bacterium with a curved rod shape, usually found in an estuary or marine environment, and causes spoilage of C. lentillifera [3].
An increasing number of microbes are being identified as pathogens of macroalgal disease [23], but bacteria attached to C. lentillifera remain largely unclear for the species composition. In addition, the consumption of the cultured C. lentillifera directly after washing with tap water is quite common [24]. Our study aims to identify bacterial communities associated with C. lentillifera by high-throughput 16S rDNA sequencing and explore whether washing with tap water can eliminate some pathogenic bacteria. Our results regarding the bacterial characteristics illustrated the structure of C. lentillifera microflora and determined the effectiveness of washing for food safety of C. lentillifera.
2 Materials and methods
2.1 Sample collection and DNA extraction
C. lentillifera samples, cultured with sand-filtered seawater pumped from the South China Sea, were collected from culture ponds in Shenzhen, Guangdong province of China (114°03′ E/22°44′ N). C. lentillifera materials were collected monthly from June 2018 to May 2019, except in January as the species was absent. Then, C. lentillifera materials collected each time were assigned to the control group (marked as S) and washed group (marked as SW). For the washed group, C. lentillifera materials were soaked with chlorinated tap water for 2 h, and the water was changed four times for 30 min each during the washing process. All the samples were stored at −80.0°C until further processing. C. lentillifera samples were named the group marker plus the collection time. For example, S1806 was collected in June 2018 and divided into the control group; and SW1905 was collected in May 2019 and divided into the washed group (Table 1).
Detail information about all samples used in this study
Samples | Group name | Subgroup name | Tag number | OTU number | Sample time | Water temperature (°C) | |
---|---|---|---|---|---|---|---|
S1806 | S | S1 | 33,742 | 1,133 | June 2018 | 28.5 | |
S1807 | S | S1 | 34,397 | 1,733 | July 2018 | 29.5 | |
S1808 | S | S1 | 40,463 | 1,433 | August 2018 | 29.0 | |
S1809 | S | S2 | 42,789 | 1,223 | September 2018 | 26.0 | |
S1810 | S | S2 | 31,559 | 1,141 | October 2018 | 24.5 | |
S1811 | S | S2 | 40,601 | 1,222 | November 2018 | 21.5 | |
S1812 | S | S3 | 41,679 | 1,160 | December 2018 | 20.5 | |
S1902 | S | S3 | 40,713 | 1,129 | February 2019 | 20.0 | |
S1903 | S | S4 | 42,186 | 719 | March 2019 | 23.0 | |
S1904 | S | S4 | 40,097 | 1,696 | April 2019 | 25.5 | |
S1905 | S | S4 | 40,377 | 1,358 | May 2019 | 27.0 | |
SW1806 | SW | SW1 | 35,689 | 1,071 | June 2018 | 28.5 | |
SW1807 | SW | SW1 | 31,833 | 1,341 | July 2018 | 29.5 | |
SW1808 | SW | SW1 | 41,677 | 1,260 | August 2018 | 29.0 | |
SW1809 | SW | SW2 | 42,573 | 1,259 | September 2018 | 26.0 | |
SW1810 | SW | SW2 | 33,145 | 1,363 | October 2018 | 24.5 | |
SW1811 | SW | SW2 | 42,496 | 510 | November 2018 | 21.5 | |
SW1812 | SW | SW3 | 35,814 | 1,474 | December 2018 | 20.5 | |
SW1902 | SW | SW3 | 45,465 | 701 | February 2019 | 20.0 | |
SW1903 | SW | SW4 | 42,498 | 820 | March 2019 | 23.0 | |
SW1904 | SW | SW4 | 40,855 | 1,507 | April 2019 | 25.5 | |
SW1905 | SW | SW4 | 43,602 | 592 | May 2019 | 27.0 |
S: control group and SW: washed group. S1, S2, S3, and S4: control C. lentillifera samples collected in summer, autumn, winter, and spring; and SW1, SW2, SW3, and SW4: washed C. lentillifera samples collected in summer, autumn, winter, and spring. All samples were collected monthly. Three replicates per season were performed.
The sampling temperature of seawater was 20.0–29.5°C with an average temperature of 25.0°C. When dividing the sampling time into four seasons, the average temperatures in summer (labeled as 1), autumn (labeled as 2), winter (labeled as 3), and spring (labeled as 4) were 29.0, 24.0, 20.25, and 25.2°C, respectively. To understand the diversities and variability of microorganisms with the change of seasons in C. lentillifera, all the samples were assigned to seasonal subgroups. Detailed information is shown in Table 1. All samples were collected monthly. Three replicates per season were performed.
For DNA extraction from C. lentillifera, TIANamp Stool DNA Kit (Tiangen, Beijing, China) was used according to the manufacturer’s protocol. The obtained DNA integrity was tested by 1% agarose gel electrophoresis and quantified using the PicoGreen dsDNA quantitation assay (Invitrogen, Carlsbad, CA), and the extracts were stored at −20.0°C.
2.2 16S rDNA library generation and microbiome sequencing
The universal primers 515F (5′-GTGCCAGCMGCCGCGGTAA-3′), together with 806R (5′-GGACTACHVGGGTWTCTAAT-3′), were used to amplify the bacterial 16S rRNA gene V4 hypervariable region of DNA samples following specific procedures. The polymerase chain reaction (PCR) reaction system consisted of 1× Hi-Fidelity buffer, 30 ng qualified genomic DNA, dNTP PurePeak DNA polymerase mix (200 µM, Pierce Nucleic Acid Technologies, Milwaukee, WI, USA), Platinum Taq High Fidelity Polymerase (1 unit, Life Technologies, Carlsbad, CA, USA), MgCl2 (2.0 mM), 0.06% BSA, along with forward and reverse primers (0.2 µM each). PCR amplification parameters were set as follows: 3 min of initial denaturation under 98.0°C; 45 s under 98.0°C, 45 s under 55.0°C, and 45 s under 72.0°C for 30 cycles; 7 min of extension under 72.0°C. Then, the Agencourt AMPure XP magnetic beads were utilized to purify the amplified PCR products, eventually dissolved into the elution buffer. The Agilent 2100 Bioanalyzer (Agilent Technologies, Santa Clara, CA, USA) was adopted to test the DNA libraries, while the HiSeq platform was used for pair-end sequencing, with the PE250 sequencing strategy was used (PE251 + 8 + 8 + 251; HiSeq SBS Kit V2, Illumina) under specific protocols.
2.3 Sequence analysis and bioinformatics
Clean data were obtained by filtering low-quality sequences from Raw fastq files using the program Quantitative Insights Into Microbial Ecology (version 1.9.1) (http://www.wernerlab.org/software/macqiime) [25], as described in an earlier study [26]. Then, Fast Length Adjustment of Short reads software (v1.2.11) [27] was used to merge those pair-end reads for obtaining tags that contained the V4 hypervariable region, the minimal matching length was 15 bp, whereas the mismatch ratio was 0.1 within the overlapped regions. UPARSE [28] was utilized to cluster the operational taxonomic units (OTUs) with a similarity threshold of 97%, whereas UCHIME [29] was used to identify and remove the chimeric sequences. The sequence NCBI number was PRJNA658212. For assigning OTUs to the nearest matching described taxon, the Greengenes taxonomy database (version 13_5) was adopted to query sequences for 16S rRNA genes [30]. Finally, each quality-filtered read was mapped by the usearch_global algorithm to the eventual set, which represented OTU sequences [31], to obtain the community composition of each sample.
In the samples, the microorganism alpha-diversity indices were evaluated according to the annotated data, including the observed species index, Chao I richness, ace index, Shannon index, and good coverage [32]. Among them, the observed species, Chao I richness, and ace index reflected the species richness of the bacterial community. The rarecurve function was used to calculate and plot the rarefaction curves [33], corresponding to the observed species in the R package vegan. Shannon index presents the diversity of microbial species and can be impacted by species evenness and richness of a sample community, while good coverage is a value representing sequencing coverage of the sample library. The relative abundance (RA) of the bacterial community composition of the samples was evaluated at the levels of phylum, class, and genus. Multiple comparisons of the bacterial alpha-diversity indices and RA between the different groups (or subgroups) were subject to one-way analysis of variance and Tukey’s HSD post hoc test using the SPSS 19.0 software. The results were presented as mean ± standard error, and differences were considered significant at p < 0.05.
Linear discriminant analysis effect size (LEfSe) [34] has been developed as an approach to discover and explain biomarkers for high-dimensional data. In LEfSe, statistical significance is applied in combination with the estimation of effective size and biological consistency. In this study, LEfSe was adopted to discover biomarkers based on microorganisms. In contrast, LEfSe analysis-derived linear discriminant analysis (LDA) scores were adopted for displaying the association across taxa by the cladogram (circular hierarchical tree) regarding those remarkably upregulated and downregulated microbial taxa between two groups. In each sample, the biomarker taxon RA was presented in straight dotted lines, and the medians and averages for subgroups were also plotted. The levels of the branch graph represent the phylum, class, order, family, and genus from the inner to the outer circles. The color codes and the letters indicate the groups and the taxa, respectively, that contribute to the uniqueness of the corresponding groups when LDA >2.0.
3 Results
3.1 Richness and diversity
In this study, we first analyzed the overall microbial diversity in a total of 22 C. lentillifera samples across four seasons. The samples were sequenced, yielding 0.86 million short-read V4 16S rRNA gene sequences (31,559–45,465 per library; Table 1). After strict quality and size filtering, high-quality sequences were clustered into 4,388 OTUs corresponding to the bacterial community (510–1,733 per sample; Table 1). Observed species rarefaction curves reached coverages of more than 0.95 (Table 2), suggesting that a very reasonable sequencing depth has been attained (Figure 1).
Average alpha-diversity indices of the different group samples
Group | Subgroup | Observed species | Chao1 richness | Ace index | Shannon index | Good coverage | |
---|---|---|---|---|---|---|---|
S | S1 | 1062.5 ± 239.6a | 1453.3 ± 273.2a | 1555.8 ± 257.5a | 4.8 ± 0.6a | 0.950 ± 0.009a | |
S2 | 867.2 ± 60.2a | 1243.1 ± 20.4a | 1365.4 ± 88.2a | 3.1 ± 0.4b | 0.958 ± 0.006a | ||
S3 | 820.8 ± 17.3a | 1213.1 ± 86.8a | 1370.4 ± 206.1a | 3.0 ± 0.5b | 0.962 ± 0.000a | ||
S4 | 910.7 ± 353.6a | 1291.3 ± 494.3a | 1448.2 ± 560.8a | 3.5 ± 0.7ab | 0.959 ± 0.013a | ||
Total | 923.9 ± 214.8 | 1308.1 ± 272.3 | 1440.8 ± 297.8 | 3.7 ± 0.9 | 0.957 ± 0.009 | ||
SW | SW1 | 889.8 ± 82.0a | 1274.3 ± 162.9a | 1399.4 ± 201.5a | 4.2 ± 05a | 0.955 ± 0.008a | |
SW2 | 759.2 ± 349.1a | 1104.3 ± 451.8a | 1215.7 ± 455.7a | 3.6 ± 1.4a | 0.962 ± 0.014a | ||
SW3 | 796.8 ± 431.9a | 1116.3 ± 517.9a | 1241.2 ± 442.3a | 3.6 ± 2.1a | 0.962 ± 0.018a | ||
SW4 | 685.4 ± 350.3a | 1045.7 ± 450.6a | 1269.5 ± 425.5a | 2.9 ± 1.1a | 0.967 ± 0.012a | ||
Total | 781.5 ± 274.6 | 1136.9 ± 349.5 | 1285.1 ± 333.6 | 3.6 ± 1.2 | 0.961 ± 0.012 |
S: control group and SW: washed group. S1, S2, S3, and S4: control C. lentillifera samples collected in summer, autumn, winter, and spring; and SW1, SW2, SW3, and SW4: washed C. lentillifera samples collected in summer, autumn, winter, and spring. The results were presented as mean ± standard error, and different letters indicate that there are significant differences among different groups (seasons) (p < 0.05).

Observed species rarefaction curves of all samples. S: control group and SW: washed group.
Among all the detected OTUs, 2,946 OTUs were shared in the S and SW groups, whereas 616 and 233 OTUs were specific in the S and SW groups, respectively (Figure S1). A total of 3,562 OTUs were found in the S group, of which 919 OTUs were shared in all seasons, whereas 411, 205, 136, and 341 OTUs were specific in summer, autumn, winter, and spring, respectively (Figure S2). Most OTUs were found in summer, followed by spring, autumn, and winter. Furthermore, a total of 3,179 OTUs was found in the SW group, with 871 OTUs shared among all the seasons, and 387, 226, 171, and 253 OTUs specific in the summer, autumn, winter, and spring, respectively, and a general lower RA than in the S group (Figure S3).
The average number of observed species, the community richness, and the community diversity in each group are shown in Table 2. As for the bacterial diversity of the S group, the average values of observed species, Chao1, ace index, and Shannon index were 923.9 ± 214.8, 1308.1 ± 272.3, 1440.8 ± 297.8, and 3.7 ± 0.9, respectively. The highest values of the richness indices and diversity indices appeared in summer, and then they decreased as the temperature decreased and, finally, increased with the arrival of spring and the rise in the temperature (Figure S4a and b). In particular, the Shannon index values in autumn and winter were significantly lower than that in summer (S1_vs_S2, p = 0.027; S1_vs_S3, p = 0.036; Figure S4b). In the samples of the SW group, the average value of observed species, Chao1, ace index, and Shannon index were 781.5 ± 274.6, 1136.9 ± 349.5, 1285.1 ± 333.6, and 3.6 ± 1.2, respectively. However, the diversity decreased compared to that in the S group, with no significant difference between the two groups (p > 0.05, Table 2). The bacterial diversity of the SW group showed a seasonal trend similar to that observed in the S group. The richness and diversity indices appeared high in the summer and decreased in autumn and winter, with the lowest values in the spring. No significant differences were observed among the seasons (Figure S4c and d). As for the bacterial diversity of the S and SW groups in the same season, the richness and diversity indices in the SW group showed no significant difference to that observed in the S groups (p > 0.05, Figure S5).
3.2 Prokaryotic community composition and relationships based on phylum, class, and genus levels in different groups
Forty-three prokaryotic phyla were detected in all the samples, wherein 41 and 39 were detected in the S and SW groups, respectively. The predominant phyla observed were Proteobacteria (68.96%), Bacteroidetes (9.20%), Planctomycetes (8.13%), Cyanobacteria (5.57%), Actinobacteria (2.72%), Chloroflexi (2.04%), Acidobacteria (0.73%), and Verrucomicrobia (0.59%), which accounted for more than 98% of all the sequences. The unclassified prokaryotic phyla constituted 0.58% of all the sequences (Table S1, Figure 2a). As shown in Figure 2a and Table S1, the five most abundant bacterial communities were Proteobacteria, Bacteroidetes, Planctomycetes, Cyanobacteria, and Actinobacteria in both S and SW groups, accounting for 69.13 and 68.80%, 10.51 and 7.88%, 7.43 and 8.83%, 4.90 and 6.25%, and 2.36 and 3.08% in S and SW groups, respectively.

Bacterial distribution in the different groups: (a) evaluated at the phylum taxonomical level, (b) evaluated at the class taxonomical level, and (c) evaluated at the genus taxonomical level. S: control group and SW: washed group.
In the total samples, 14 prokaryotic classes were detected in addition to others (RA less than 0.5% in all the samples) (4.22%), and the unclassified prokaryote at the class level accounted for 1.82% of all sequences (Table S1). The RAs of prokaryotes at the Class level in different groups are shown in Figure 2b. Alphaproteobacteria (Proteobacteria) and Gammaproteobacteria (Proteobacteria) were the most and the second most predominant classes, respectively. Alphaproteobacteria accounted for 57.34 and 58.43% of the reads, and Gammaproteobacteria accounted for 8.97 and 8.18% of the reads in the S and SW groups, respectively. The dominant bacterial communities in the S group also included Planctomycetia (Planctomycetes), Saprospirae (Spirochaetes), and Flavobacteriia (Bacteroidetes), accounting for 5.51, 3.84, and 3.55%, respectively (Table S1 and Figure 2b). The dominant bacterial communities in the SW group also included Planctomycetia, Synechococcophycideae (Cyanobacteria), and Acidimicrobiia (Actinobacteria), accounting for 7.41, 5.27, and 3.03%, respectively (Table S1 and Figure 2b).
Only five prokaryotic genera were detected in all the samples in addition to others (6.89%), and the unclassified prokaryote at the genus level accounted for 85.53% of all the sequences (Table S1). The RA of prokaryotes at the genus level in different groups is shown in Figure 2c. The S group was dominated by Planctomyces (Planctomycetia, Planctomycetes; 1.27%) and Lyngbya (Cyanobacteria, Cyanophyta; 1.25%), and the SW group was dominated by Labrenzia (Alphaproteobacteria, Proteobacteria; 8.11%) and Planctomyces (1.72%) apart from those unclassified ones (Table S1 and Figure 2c).
For better understanding, the relationship between the bacterial community and the diverse structures of those treated C. lentillifera, this study conducted LEfSe analysis for determining those high-dimensional biomarker bacterial taxa of S versus SW samples (Figure 3a). Then, the cladogram (Figure 3b) was constructed to display the associations among the biomarker taxa. The results revealed that at the phylum level, Bacteroidetes was a biomarker bacteria related to the S group. At the class level, Flavobacteriia, Deltaproteobacteria (Proteobacteria), and Gammaproteobacteria were associated with the S group, and Alphaproteobacteria was associated with the SW group. The high-dimensional biomarker genera, such as Owenweeksia (Flavobacteriia, Bacteroidetes), Flavobacterium (Flavobacteriia, Bacteroidetes), Thalassospira (Alphaproteobacteria, Proteobacteria), Marivita (Alphaproteobacteria, Proteobacteria), Ruegeria (Alphaproteobacteria, Proteobacteria), Haliangiaceae (Deltaproteobacteria, Proteobacteria), Plesiocystis (Deltaproteobacteria, Proteobacteria), Alteromonas (Gammaproteobacteria, Proteobacteria), Glaciecola (Gammaproteobacteria, Proteobacteria), Congregibacter (Gammaproteobacteria, Proteobacteria), Hahella (Gammaproteobacteria, Proteobacteria), Enterovibrio (Gammaproteobacteria, Proteobacteria), and Vibrio (Gammaproteobacteria, Proteobacteria), were associated with S group, and genera Labrenzia and Acinetobacter (Gammaproteobacteria, Proteobacteria) were related to SW group (Figure 3). As mentioned above, only Labrenzia has a RA of more than 0.5% in the groups.

LEfSe analysis in S and SW groups: (a) LDA scores (log 10) derived from LEfSe analysis, showing the biomarker taxa for S and SW and (b) cladogram generated from LEfSe analysis showing the relationship between taxon. S: control group and SW: washed group.
3.3 Changes in the bacterial communities in two groups across the seasons
The distribution of the dominant bacterial groups in the main phyla exhibited no changes across seasons for S and SW groups. Proteobacteria, Bacteroidetes, Planctomycetes, Cyanobacteria, and Actinobacteria were listed among the top five bacterial communities in different seasons (Table 3). In the S group, the abundance of Planctomycetes was the highest in summer, which decreased significantly in the other three seasons (S1_vs_S2, p = 0.007; S1_vs_S3, p = 0.006; and S1_vs_S4, p = 0.004; Figure S6a). Other dominant bacterial communities showed no significant temporal differences in the S group (p > 0.05, Table 3). In addition, the abundance of dominant bacterial communities showed no significant difference among these four seasons in the SW group (p > 0.05, Table 3).
The main abundant bacterial phyla associated with the S and SW across seasons
Group | Subgroup | Proteobacteria | Bacteroidetes | Planctomycetes | Cyanobacteria | Actinobacteria |
---|---|---|---|---|---|---|
S | S1 | 52.7 ± 10.7a | 10.9 ± 2.9a | 14.0 ± 3.5a | 7.0 ± 10.6a | 5.0 ± 3.7a |
S2 | 77.6 ± 6.6a | 8.8 ± 2.6a | 5.9 ± 0.9b | 2.8 ± 3.7a | 1.3 ± 0.2a | |
S3 | 77.6 ± 7.2a | 8.2 ± 1.9a | 4.7 ± 1.1b | 3.6 ± 2.0a | 1.6 ± 0.3a | |
S4 | 69.2 ± 11.8a | 13.6 ± 6.2a | 5.1 ± 0.8b | 6.1 ± 7.9a | 1.7 ± 1.3a | |
SW | SW1 | 55.1 ± 13.0a | 10.0 ± 3.0a | 12.3 ± 6.9a | 9.8 ± 15.5a | 4.8 ± 4.5a |
SW2 | 67.9 ± 14.2a | 10.0 ± 6.6a | 10.5 ± 4.8a | 2.2 ± 2.1a | 3.9 ± 1.1a | |
SW3 | 71.9 ± 24.8a | 6.4 ± 6.0a | 8.4 ± 5.9a | 6.6 ± 8.3a | 2.5 ± 0.6a | |
SW4 | 75.7 ± 17.0a | 5.8 ± 5.0a | 5.2 ± 3.2a | 8.4 ± 13.3a | 1.3 ± 1.2a |
S: control group and SW: washed group. S1, S2, S3, and S4: control C. lentillifera samples collected in summer, autumn, winter, and spring; and SW1, SW2, SW3, and SW4: washed C. lentillifera samples collected in summer, autumn, winter, and spring. The results were presented as mean ± standard error, and different letters indicate that there are significant differences among different groups (seasons) (p < 0.05).
The top five ranked dominant bacterial groups belonging to the main classes exhibited slight changes in the S group. The most and the second most predominant bacterial communities observed in the S group for all the seasons were Alphaproteobacteria (35.4–70.4%) and Gammaproteobacteria (5.4–11.5%), respectively (Table 4). In addition, Planctomycetia (9.8%), Synechococcophycideae (5.2%), and Acidimicrobiia (4.9%) were the other three dominant bacterial classes observed in summer; Planctomycetia (4.4 and 3.8%, respectively), Saprospirae (3.7 and 4.4%, respectively), and Flavobacteriia (2.5 and 2.0%, respectively) were dominant bacterial classes in autumn and winter. In comparison, Flavobacteriia (6.1%), Saprospirae (4.2%), and Planctomycetia (4.0%) were dominant bacterial classes in spring (Table 4). Among these dominant bacterial classes in the S group, the abundance of Alphaproteobacteria was the lowest in summer, increased significantly in autumn (p = 0.02) and winter (p = 0.022), and then decreased again with the spring coming (Table 4 and Figure S6b). Differently, Planctomycetia showed the highest abundance in summer, which significantly decreased in the other three seasons (S1_vs_S2, p = 0.019; S1_vs_S3, p = 0.019; and S1_vs_S4, p = 0.013; Table 4 and Figure S6b). Other dominant bacterial classes demonstrated no different abundances across seasons (p > 0.05, Table 4).
The main abundant bacterial class associated with the S and SW across seasons
Group | Subgroup | Alphaproteobacteria | Gammaproteobacteria | Planctomycetia | Synechococcophycideae | Saprospirae | Acidimicrobiia | Flavobacteriia | Anaerolineae |
---|---|---|---|---|---|---|---|---|---|
S | S1 | 35.4 ± 14.4a | 11.5 ± 3.8a | 9.8 ± 2.9a | 5.2 ± 8.1a | 3.3 ± 0.5a | 4.9 ± 3.7a | 3.0 ± 1.9a | 3.8 ± 1.9a |
S2 | 67.3 ± 5.2b | 8.6 ± 2.6a | 4.4 ± 0.5b | 1.1 ± 1.4a | 3.7 ± 1.5a | 1.2 ± 0.2a | 2.5 ± 0.4a | 0.2 ± 0.2b | |
S3 | 70.4 ± 7.7b | 5.4 ± 0.1a | 3.8 ± 0.4b | 1.9 ± 0.3a | 4.4 ± 0.5a | 1.5 ± 0.3a | 2.0 ± 1.4a | 1.6 ± 1.0ab | |
S4 | 57.8 ± 8.1ab | 9.4 ± 4.6a | 4.0 ± 0.7b | 1.8 ± 1.6a | 4.2 ± 2.8a | 1.6 ± 1.3a | 6.1 ± 5.2a | 1.7 ± 0.5ab | |
SW | SW1 | 42.3 ± 17.3a | 9.3 ± 5.1a | 9.8 ± 6.7a | 8.8 ± 14.3a | 4.0 ± 1.1a | 4.7 ± 4.4a | 2.5 ± 0.7a | 3.5 ± 2.4a |
SW2 | 58.4 ± 18.1a | 7.6 ± 2.8a | 9.1 ± 3.6a | 1.2 ± 1.1a | 4.8 ± 4.1a | 3.9 ± 1.1a | 1.3 ± 0.7a | 2.5 ± 2.7a | |
SW3 | 58.6 ± 36.1a | 10.9 ± 9.5a | 7.2 ± 5.2a | 4.8 ± 5.9a | 2.1 ± 2.3a | 2.5 ± 0.6a | 1.6 ± 0.7a | 0.8 ± 0.5a | |
SW4 | 67.7 ± 21.6a | 6.7 ± 4.3a | 4.4 ± 2.7a | 7.8 ± 12.4a | 1.4 ± 1.2a | 1.2 ± 1.2a | 1.6 ± 1.1a | 2.1 ± 2.0a |
S: control group and SW: washed group. S1, S2, S3, and S4: control C. lentillifera samples collected in summer, autumn, winter, and spring; and SW1, SW2, SW3, and SW4: washed C. lentillifera samples collected in summer, autumn, winter, and spring. The results were presented as mean ± standard error, and different letters indicate that there are significant differences among different groups (seasons) (p < 0.05).
In the SW group, the dominant bacterial groups belonging to the main classes observed in summer were Alphaproteobacteria (42.3%), Planctomycetia (9.8%), Gammaproteobacteria (9.3%), Synechococcophycideae (8.8%), and Acidimicrobiia (4.7%). In autumn, the dominant bacterial communities were Alphaproteobacteria (58.4%), Planctomycetia (9.1%), Gammaproteobacteria (7.6%), Saprospirae (4.8%), and Acidimicrobiia (3.9%). In winter, the dominant bacterial communities were Alphaproteobacteria (58.6%), Gammaproteobacteria (10.9%), Planctomycetia (7.2%), Synechococcophycideae (4.8%), and Acidimicrobiia (2.5%). In spring, the dominant bacterial communities were Alphaproteobacteria (67.7%), Synechococcophycideae (7.8%), Gammaproteobacteria (6.7%), Planctomycetia (4.4%), and Anaerolineae (2.1%) (Table 4). However, there were no significant differences in the bacterial abundance across seasons in the SW group (p > 0.05, Table 4).
4 Discussion
A macroalgal community contains bacteria, fungi, diatoms, protozoa, spores, and larvae of marine invertebrates [35]. Among these attaching organisms, many bacteria and fungi have been identified as pathogens of macroalgal diseases [23]. However, bacteria show high abundance in the primary colonizers [36], whereas fungi are relatively rare in the sea [37]. In this study, the seasonal time-series autocorrelation of bacterial diversity in C. lentillifera was conducted by high-throughput 16S rDNA sequencing and revealed that washing with tap water slightly alters the microbiome of C. lentillifera.
Overall, in the present study, 5 major genera and 14 major classes of bacteria were detected in 43 phyla in C. lentillifera (Table S1). Proteobacteria and Bacteroidetes constituted the most abundant bacterial phyla associated with C. lentillifera, which was consistent with the earlier studies on other seaweeds [38,39], such as Laminaria saccharina [39], L. hyperborea [40], Ulva australis [41], C. racemosa [42], Cystoseira compressa [43], and Sargassum muticum [44]. Alphaproteobacteria and Gammaproteobacteria were the most and the second most predominant classes related to C. lentillifera, accounting for an average of 57.89 and 8.58% of the reads in the S and SW groups, respectively. While at the genus level, only five main prokaryotic genera were detected in addition to others (6.89%), and the abundance of unclassified prokaryote reached to 85.53% (Table S1), which needs to be further studied.
Temporal variations of C. lentillifera-related bacterial microbial taxonomic composition were measured. The highest diversity of the C. lentillifera bacterial community was revealed in summer, followed by spring, autumn, and winter, respectively, according to OUT richness and alpha diversity (Table 2), indicating that the bacterial diversity increases with the temperature of seasons. However, no significant temporal differences were found in the bacterial structure in C. lentillifera, which may be due to the relatively stable temperature of Shenzhen throughout the year. Shenzhen (113°46′–114°37′ E, 22°27′–22°52′ N), one of the coastal cities in the south of China and near Hong Kong, has a mild climate with an annual average temperature of 23.0°C. The sampling temperature of seawater in this study was 20.0–29.5°C with an average temperature of 25.0°C, with a small shift across seasons. In addition, slight changes of the dominant bacterial groups contributed most of the dissimilarity across the seasons in C. lentillifera. The most pronounced temporal changes in the microbial community of C. lentillifera were abundantly increased in Planctomycetes in summer (Table 3), which occurred primarily due to the increase of Planctomycetia (Table 4). Planctomycetes have been recognized as capable of mineralizing organic matters into inorganic counterparts, which fulfills the nutritional demands of the macroalgae [45,46,47]. Meanwhile, macroalgae are rich in Planctomycetes [47,48], the RA of which varies greatly depending on seaweed species and seasons [35]. The summer increase of Planctomycetes in the present study is congruent with the studies reported on L. hyperborean [40] and Sargassum muticum [44].
To our knowledge, this is the first study to investigate whether washing with tap water alters the microbiome associated with C. lentillifera using high-throughput 16S rRNA gene sequencing and modern multivariate data analyzing software programs. The LEfSe analysis and cladogram visualization (Figure 3) revealed few types of biomarker bacteria associated with washed C. lentillifera, and the most representative one was Labrenzia. The RA of the genus Labrenzia, belonging to the family Rhodobacteraceae, was 50 times higher in C. lentillifera after washing. Labrenzia is the aerobic anoxygenic phototrophic bacterium that can generate little bacteriochlorophyll [49]. The abundance of Labrenzia was found to be higher in healthy C. lentillifera as compared to the diseased samples, which may contribute to the photosynthesis of algae [50]. Because the genus Labrenzia was difficult to elute by tap water, it resulted in an increased abundance in C. lentillifera even after washing, suggesting that there might be a symbiotic relationship between C. lentillifera and Labrenzia.
In China, the consumption of C. lentillifera directly after washing is quite common, which might lead to be bacterial infection. More types of high-dimensional biomarkers bacteria at different levels were associated with the S group, such as phylum of Bacteroidetes, classes of Flavobacteriia, Flavobacterium, Deltaproteobacteria, and Gammaproteobacteria, and genera of Haliangiaceae, Plesiocystis, Alteromonas, Glaciecola, or Congregibacter (Figure 3). The abundance of these bacteria significantly decreased in C. lentillifera after washing, indicating that the bacterial groups were on the surface of C. lentillifera and relatively easy to elute by tap water. In the current study, Vibrio was one of the representatives of high-dimensional biomarker genera associated with the S group. It significantly decreased abundance in C. lentillifera after washing, which benefits consumers’ health, as it could cause seafood-borne diseases (Figure 3). For example, Vibrio cholerae is the pathogen causing human cholera. These ancient and widespread infectious diseases have caused many epidemics worldwide, mainly manifested as severe vomiting, diarrhea, water loss, and high mortality, and are considered an international quarantine infectious disease [51]. V. parahaemolyticus is another species belonging to the Vibrio genera. Eating food containing these bacteria can cause food poisoning, also known as halophilic bacteria food poisoning, the main clinical symptoms of which are acute onset, abdominal pain, vomiting, diarrhea, and watery stool [52].
Although LEfSe analysis revealed that the abundances of some bacteria groups associated with C. lentillifera were significantly decreased after washing with tap water, there was only a marginal reduction in both richness and diversity of the entire bacterial communities according to the results of α-diversity (Table 2). It was notable that there were 233 OTUs specific for the SW group (Figure S1), which may come from the tap water microbiome used for washing, or it may be caused by individual differences. The reduction in the abundance of harmful bacteria (such as Vibrio) in this study showed that washing C. lentillifera with tap water had a certain positive significance for food safety. In addition, there were still relatively abundant bacterial communities in C. lentillifera after washing with tap water, which may have hidden dangers to food safety, and more effective cleaning methods need to be explored. However, the results obtained by high-throughput sequencing in this study should be validated by specific and dedicated assays (microbial culture techniques or PCR), and specific norms for microbial food safety tasks need to be applied in the future.
5 Conclusion
In this study, a total of 4,388 OTUs were obtained from all the samples, and 5 major genera and 14 major classes of bacteria were detected in 43 phyla in C. lentillifera. The predominant prokaryotic phyla were Proteobacteria, Bacteroidetes, Planctomycetes, Cyanobacteria, Actinobacteria, Verrucomicrobia, Chloroflexi, and Acidobacteria. We demonstrated that the bacterial diversities associated with C. lentillifera increase with the temperature of seasons, with no significant temporal shifts. Slight changes in the dominant bacterial groups contributed most of the dissimilarity in bacterial communities across the seasons in C. lentillifera. For instance, the abundance of Planctomycetes in C. lentillifera was significantly increased in summer than in the other three seasons, which occurred mostly due to the increase of Planctomycetia. The increased abundance of Labrenzia in washed C. lentillifera suggested that there was a symbiotic relationship between C. lentillifera and Labrenzia. In contrast, the significant reduction in the abundance of harmful bacteria (such as Vibrio) showed that washing C. lentillifera with tap water is beneficial for human health. However, we found that both the richness and diversity of the bacterial communities associated with C. lentillifera only slightly decreased after washing with tap water, indicating hidden dangers in C. lentillifera for food safety, and more effective cleaning methods need to be explored.
Acknowledgments
We thank the technical support from the Beijing Genomics Institute.
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Funding information: This research was supported by Shenzhen Science and Technology Project “Studies on cultivation ecology of macroalgae with high value and key basic questions about food safety” (JCYJ20170818140317993), Post-doctoral Foundation Project of Shenzhen Polytechnic (6019330003K), and Post-doctoral Foundation Project of Shenzhen Polytechnic (6019330004K).
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Author contributions: Conceptualization: Zhili Huang, and Gang Jin; validation: Meixia Pang, Le Lv, and Xiaodong Li; resources: Zhili Huang; data curation, Meixia Pang; writing – original draft preparation: Meixia Pang; writing – review and editing: Gang Jin; project administration: Gang Jin; and funding acquisition: Gang Jin and Meixia Pang. All authors have read and agreed to the published version of the manuscript.
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Conflict of interest: Authors state no conflict of interest.
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Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
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- Effects of the interaction of Notch and TLR4 pathways on inflammation and heart function in septic heart
- Monosodium iodoacetate-induced subchondral bone microstructure and inflammatory changes in an animal model of osteoarthritis
- A rare presentation of type II Abernethy malformation and nephrotic syndrome: Case report and review
- Rapid death due to pulmonary epithelioid haemangioendothelioma in several weeks: A case report
- Hepatoprotective role of peroxisome proliferator-activated receptor-α in non-cancerous hepatic tissues following transcatheter arterial embolization
- Correlation between peripheral blood lymphocyte subpopulations and primary systemic lupus erythematosus
- A novel SLC8A1-ALK fusion in lung adenocarcinoma confers sensitivity to alectinib: A case report
- β-Hydroxybutyrate upregulates FGF21 expression through inhibition of histone deacetylases in hepatocytes
- Identification of metabolic genes for the prediction of prognosis and tumor microenvironment infiltration in early-stage non-small cell lung cancer
- BTBD10 inhibits glioma tumorigenesis by downregulating cyclin D1 and p-Akt
- Mucormycosis co-infection in COVID-19 patients: An update
- Metagenomic next-generation sequencing in diagnosing Pneumocystis jirovecii pneumonia: A case report
- Long non-coding RNA HOXB-AS1 is a prognostic marker and promotes hepatocellular carcinoma cells’ proliferation and invasion
- Preparation and evaluation of LA-PEG-SPION, a targeted MRI contrast agent for liver cancer
- Proteomic analysis of the liver regulating lipid metabolism in Chaohu ducks using two-dimensional electrophoresis
- Nasopharyngeal tuberculosis: A case report
- Characterization and evaluation of anti-Salmonella enteritidis activity of indigenous probiotic lactobacilli in mice
- Aberrant pulmonary immune response of obese mice to periodontal infection
- Bacteriospermia – A formidable player in male subfertility
- In silico and in vivo analysis of TIPE1 expression in diffuse large B cell lymphoma
- Effects of KCa channels on biological behavior of trophoblasts
- Interleukin-17A influences the vulnerability rather than the size of established atherosclerotic plaques in apolipoprotein E-deficient mice
- Multiple organ failure and death caused by Staphylococcus aureus hip infection: A case report
- Prognostic signature related to the immune environment of oral squamous cell carcinoma
- Primary and metastatic squamous cell carcinoma of the thyroid gland: Two case reports
- Neuroprotective effects of crocin and crocin-loaded niosomes against the paraquat-induced oxidative brain damage in rats
- Role of MMP-2 and CD147 in kidney fibrosis
- Geometric basis of action potential of skeletal muscle cells and neurons
- Babesia microti-induced fulminant sepsis in an immunocompromised host: A case report and the case-specific literature review
- Role of cerebellar cortex in associative learning and memory in guinea pigs
- Application of metagenomic next-generation sequencing technique for diagnosing a specific case of necrotizing meningoencephalitis caused by human herpesvirus 2
- Case report: Quadruple primary malignant neoplasms including esophageal, ureteral, and lung in an elderly male
- Long non-coding RNA NEAT1 promotes angiogenesis in hepatoma carcinoma via the miR-125a-5p/VEGF pathway
- Osteogenic differentiation of periodontal membrane stem cells in inflammatory environments
- Knockdown of SHMT2 enhances the sensitivity of gastric cancer cells to radiotherapy through the Wnt/β-catenin pathway
- Continuous renal replacement therapy combined with double filtration plasmapheresis in the treatment of severe lupus complicated by serious bacterial infections in children: A case report
- Simultaneous triple primary malignancies, including bladder cancer, lymphoma, and lung cancer, in an elderly male: A case report
- Preclinical immunogenicity assessment of a cell-based inactivated whole-virion H5N1 influenza vaccine
- One case of iodine-125 therapy – A new minimally invasive treatment of intrahepatic cholangiocarcinoma
- S1P promotes corneal trigeminal neuron differentiation and corneal nerve repair via upregulating nerve growth factor expression in a mouse model
- Early cancer detection by a targeted methylation assay of circulating tumor DNA in plasma
- Calcifying nanoparticles initiate the calcification process of mesenchymal stem cells in vitro through the activation of the TGF-β1/Smad signaling pathway and promote the decay of echinococcosis
- Evaluation of prognostic markers in patients infected with SARS-CoV-2
- N6-Methyladenosine-related alternative splicing events play a role in bladder cancer
- Characterization of the structural, oxidative, and immunological features of testis tissue from Zucker diabetic fatty rats
- Effects of glucose and osmotic pressure on the proliferation and cell cycle of human chorionic trophoblast cells
- Investigation of genotype diversity of 7,804 norovirus sequences in humans and animals of China
- Characteristics and karyotype analysis of a patient with turner syndrome complicated with multiple-site tumors: A case report
- Aggravated renal fibrosis is positively associated with the activation of HMGB1-TLR2/4 signaling in STZ-induced diabetic mice
- Distribution characteristics of SARS-CoV-2 IgM/IgG in false-positive results detected by chemiluminescent immunoassay
- SRPX2 attenuated oxygen–glucose deprivation and reperfusion-induced injury in cardiomyocytes via alleviating endoplasmic reticulum stress-induced apoptosis through targeting PI3K/Akt/mTOR axis
- Aquaporin-8 overexpression is involved in vascular structure and function changes in placentas of gestational diabetes mellitus patients
- Relationship between CRP gene polymorphisms and ischemic stroke risk: A systematic review and meta-analysis
- Effects of growth hormone on lipid metabolism and sexual development in pubertal obese male rats
- Cloning and identification of the CTLA-4IgV gene and functional application of vaccine in Xinjiang sheep
- Antitumor activity of RUNX3: Upregulation of E-cadherin and downregulation of the epithelial–mesenchymal transition in clear-cell renal cell carcinoma
- PHF8 promotes osteogenic differentiation of BMSCs in old rat with osteoporosis by regulating Wnt/β-catenin pathway
- A review of the current state of the computer-aided diagnosis (CAD) systems for breast cancer diagnosis
- Bilateral dacryoadenitis in adult-onset Still’s disease: A case report
- A novel association between Bmi-1 protein expression and the SUVmax obtained by 18F-FDG PET/CT in patients with gastric adenocarcinoma
- The role of erythrocytes and erythroid progenitor cells in tumors
- Relationship between platelet activation markers and spontaneous abortion: A meta-analysis
- Abnormal methylation caused by folic acid deficiency in neural tube defects
- Silencing TLR4 using an ultrasound-targeted microbubble destruction-based shRNA system reduces ischemia-induced seizures in hyperglycemic rats
- Plant Sciences
- Seasonal succession of bacterial communities in cultured Caulerpa lentillifera detected by high-throughput sequencing
- Cloning and prokaryotic expression of WRKY48 from Caragana intermedia
- Novel Brassica hybrids with different resistance to Leptosphaeria maculans reveal unbalanced rDNA signal patterns
- Application of exogenous auxin and gibberellin regulates the bolting of lettuce (Lactuca sativa L.)
- Phytoremediation of pollutants from wastewater: A concise review
- Genome-wide identification and characterization of NBS-encoding genes in the sweet potato wild ancestor Ipomoea trifida (H.B.K.)
- Alleviative effects of magnetic Fe3O4 nanoparticles on the physiological toxicity of 3-nitrophenol to rice (Oryza sativa L.) seedlings
- Selection and functional identification of Dof genes expressed in response to nitrogen in Populus simonii × Populus nigra
- Study on pecan seed germination influenced by seed endocarp
- Identification of active compounds in Ophiopogonis Radix from different geographical origins by UPLC-Q/TOF-MS combined with GC-MS approaches
- The entire chloroplast genome sequence of Asparagus cochinchinensis and genetic comparison to Asparagus species
- Genome-wide identification of MAPK family genes and their response to abiotic stresses in tea plant (Camellia sinensis)
- Selection and validation of reference genes for RT-qPCR analysis of different organs at various development stages in Caragana intermedia
- Cloning and expression analysis of SERK1 gene in Diospyros lotus
- Integrated metabolomic and transcriptomic profiling revealed coping mechanisms of the edible and medicinal homologous plant Plantago asiatica L. cadmium resistance
- A missense variant in NCF1 is associated with susceptibility to unexplained recurrent spontaneous abortion
- Assessment of drought tolerance indices in faba bean genotypes under different irrigation regimes
- The entire chloroplast genome sequence of Asparagus setaceus (Kunth) Jessop: Genome structure, gene composition, and phylogenetic analysis in Asparagaceae
- Food Science
- Dietary food additive monosodium glutamate with or without high-lipid diet induces spleen anomaly: A mechanistic approach on rat model
- Binge eating disorder during COVID-19
- Potential of honey against the onset of autoimmune diabetes and its associated nephropathy, pancreatitis, and retinopathy in type 1 diabetic animal model
- FTO gene expression in diet-induced obesity is downregulated by Solanum fruit supplementation
- Physical activity enhances fecal lactobacilli in rats chronically drinking sweetened cola beverage
- Supercritical CO2 extraction, chemical composition, and antioxidant effects of Coreopsis tinctoria Nutt. oleoresin
- Functional constituents of plant-based foods boost immunity against acute and chronic disorders
- Effect of selenium and methods of protein extraction on the proteomic profile of Saccharomyces yeast
- Microbial diversity of milk ghee in southern Gansu and its effect on the formation of ghee flavor compounds
- Ecology and Environmental Sciences
- Effects of heavy metals on bacterial community surrounding Bijiashan mining area located in northwest China
- Microorganism community composition analysis coupling with 15N tracer experiments reveals the nitrification rate and N2O emissions in low pH soils in Southern China
- Genetic diversity and population structure of Cinnamomum balansae Lecomte inferred by microsatellites
- Preliminary screening of microplastic contamination in different marine fish species of Taif market, Saudi Arabia
- Plant volatile organic compounds attractive to Lygus pratensis
- Effects of organic materials on soil bacterial community structure in long-term continuous cropping of tomato in greenhouse
- Effects of soil treated fungicide fluopimomide on tomato (Solanum lycopersicum L.) disease control and plant growth
- Prevalence of Yersinia pestis among rodents captured in a semi-arid tropical ecosystem of south-western Zimbabwe
- Effects of irrigation and nitrogen fertilization on mitigating salt-induced Na+ toxicity and sustaining sea rice growth
- Bioengineering and Biotechnology
- Poly-l-lysine-caused cell adhesion induces pyroptosis in THP-1 monocytes
- Development of alkaline phosphatase-scFv and its use for one-step enzyme-linked immunosorbent assay for His-tagged protein detection
- Development and validation of a predictive model for immune-related genes in patients with tongue squamous cell carcinoma
- Agriculture
- Effects of chemical-based fertilizer replacement with biochar-based fertilizer on albic soil nutrient content and maize yield
- Genome-wide identification and expression analysis of CPP-like gene family in Triticum aestivum L. under different hormone and stress conditions
- Agronomic and economic performance of mung bean (Vigna radiata L.) varieties in response to rates of blended NPS fertilizer in Kindo Koysha district, Southern Ethiopia
- Influence of furrow irrigation regime on the yield and water consumption indicators of winter wheat based on a multi-level fuzzy comprehensive evaluation
- Discovery of exercise-related genes and pathway analysis based on comparative genomes of Mongolian originated Abaga and Wushen horse
- Lessons from integrated seasonal forecast-crop modelling in Africa: A systematic review
- Evolution trend of soil fertility in tobacco-planting area of Chenzhou, Hunan Province, China
- Animal Sciences
- Morphological and molecular characterization of Tatera indica Hardwicke 1807 (Rodentia: Muridae) from Pothwar, Pakistan
- Research on meat quality of Qianhua Mutton Merino sheep and Small-tail Han sheep
- SI: A Scientific Memoir
- Suggestions on leading an academic research laboratory group
- My scientific genealogy and the Toronto ACDC Laboratory, 1988–2022
- Erratum
- Erratum to “Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study”
- Erratum to “A two-microRNA signature predicts the progression of male thyroid cancer”
- Retraction
- Retraction of “Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis”
Artikel in diesem Heft
- Biomedical Sciences
- Effects of direct oral anticoagulants dabigatran and rivaroxaban on the blood coagulation function in rabbits
- The mother of all battles: Viruses vs humans. Can humans avoid extinction in 50–100 years?
- Knockdown of G1P3 inhibits cell proliferation and enhances the cytotoxicity of dexamethasone in acute lymphoblastic leukemia
- LINC00665 regulates hepatocellular carcinoma by modulating mRNA via the m6A enzyme
- Association study of CLDN14 variations in patients with kidney stones
- Concanavalin A-induced autoimmune hepatitis model in mice: Mechanisms and future outlook
- Regulation of miR-30b in cancer development, apoptosis, and drug resistance
- Informatic analysis of the pulmonary microecology in non-cystic fibrosis bronchiectasis at three different stages
- Swimming attenuates tumor growth in CT-26 tumor-bearing mice and suppresses angiogenesis by mediating the HIF-1α/VEGFA pathway
- Characterization of intestinal microbiota and serum metabolites in patients with mild hepatic encephalopathy
- Functional conservation and divergence in plant-specific GRF gene family revealed by sequences and expression analysis
- Application of the FLP/LoxP-FRT recombination system to switch the eGFP expression in a model prokaryote
- Biomedical evaluation of antioxidant properties of lamb meat enriched with iodine and selenium
- Intravenous infusion of the exosomes derived from human umbilical cord mesenchymal stem cells enhance neurological recovery after traumatic brain injury via suppressing the NF-κB pathway
- Effect of dietary pattern on pregnant women with gestational diabetes mellitus and its clinical significance
- Potential regulatory mechanism of TNF-α/TNFR1/ANXA1 in glioma cells and its role in glioma cell proliferation
- Effect of the genetic mutant G71R in uridine diphosphate-glucuronosyltransferase 1A1 on the conjugation of bilirubin
- Quercetin inhibits cytotoxicity of PC12 cells induced by amyloid-beta 25–35 via stimulating estrogen receptor α, activating ERK1/2, and inhibiting apoptosis
- Nutrition intervention in the management of novel coronavirus pneumonia patients
- circ-CFH promotes the development of HCC by regulating cell proliferation, apoptosis, migration, invasion, and glycolysis through the miR-377-3p/RNF38 axis
- Bmi-1 directly upregulates glucose transporter 1 in human gastric adenocarcinoma
- Lacunar infarction aggravates the cognitive deficit in the elderly with white matter lesion
- Hydroxysafflor yellow A improved retinopathy via Nrf2/HO-1 pathway in rats
- Comparison of axon extension: PTFE versus PLA formed by a 3D printer
- Elevated IL-35 level and iTr35 subset increase the bacterial burden and lung lesions in Mycobacterium tuberculosis-infected mice
- A case report of CAT gene and HNF1β gene variations in a patient with early-onset diabetes
- Study on the mechanism of inhibiting patulin production by fengycin
- SOX4 promotes high-glucose-induced inflammation and angiogenesis of retinal endothelial cells by activating NF-κB signaling pathway
- Relationship between blood clots and COVID-19 vaccines: A literature review
- Analysis of genetic characteristics of 436 children with dysplasia and detailed analysis of rare karyotype
- Bioinformatics network analyses of growth differentiation factor 11
- NR4A1 inhibits the epithelial–mesenchymal transition of hepatic stellate cells: Involvement of TGF-β–Smad2/3/4–ZEB signaling
- Expression of Zeb1 in the differentiation of mouse embryonic stem cell
- Study on the genetic damage caused by cadmium sulfide quantum dots in human lymphocytes
- Association between single-nucleotide polymorphisms of NKX2.5 and congenital heart disease in Chinese population: A meta-analysis
- Assessment of the anesthetic effect of modified pentothal sodium solution on Sprague-Dawley rats
- Genetic susceptibility to high myopia in Han Chinese population
- Potential biomarkers and molecular mechanisms in preeclampsia progression
- Silencing circular RNA-friend leukemia virus integration 1 restrained malignancy of CC cells and oxaliplatin resistance by disturbing dyskeratosis congenita 1
- Endostar plus pembrolizumab combined with a platinum-based dual chemotherapy regime for advanced pulmonary large-cell neuroendocrine carcinoma as a first-line treatment: A case report
- The significance of PAK4 in signaling and clinicopathology: A review
- Sorafenib inhibits ovarian cancer cell proliferation and mobility and induces radiosensitivity by targeting the tumor cell epithelial–mesenchymal transition
- Characterization of rabbit polyclonal antibody against camel recombinant nanobodies
- Active legumain promotes invasion and migration of neuroblastoma by regulating epithelial-mesenchymal transition
- Effect of cell receptors in the pathogenesis of osteoarthritis: Current insights
- MT-12 inhibits the proliferation of bladder cells in vitro and in vivo by enhancing autophagy through mitochondrial dysfunction
- Study of hsa_circRNA_000121 and hsa_circRNA_004183 in papillary thyroid microcarcinoma
- BuyangHuanwu Decoction attenuates cerebral vasospasm caused by subarachnoid hemorrhage in rats via PI3K/AKT/eNOS axis
- Effects of the interaction of Notch and TLR4 pathways on inflammation and heart function in septic heart
- Monosodium iodoacetate-induced subchondral bone microstructure and inflammatory changes in an animal model of osteoarthritis
- A rare presentation of type II Abernethy malformation and nephrotic syndrome: Case report and review
- Rapid death due to pulmonary epithelioid haemangioendothelioma in several weeks: A case report
- Hepatoprotective role of peroxisome proliferator-activated receptor-α in non-cancerous hepatic tissues following transcatheter arterial embolization
- Correlation between peripheral blood lymphocyte subpopulations and primary systemic lupus erythematosus
- A novel SLC8A1-ALK fusion in lung adenocarcinoma confers sensitivity to alectinib: A case report
- β-Hydroxybutyrate upregulates FGF21 expression through inhibition of histone deacetylases in hepatocytes
- Identification of metabolic genes for the prediction of prognosis and tumor microenvironment infiltration in early-stage non-small cell lung cancer
- BTBD10 inhibits glioma tumorigenesis by downregulating cyclin D1 and p-Akt
- Mucormycosis co-infection in COVID-19 patients: An update
- Metagenomic next-generation sequencing in diagnosing Pneumocystis jirovecii pneumonia: A case report
- Long non-coding RNA HOXB-AS1 is a prognostic marker and promotes hepatocellular carcinoma cells’ proliferation and invasion
- Preparation and evaluation of LA-PEG-SPION, a targeted MRI contrast agent for liver cancer
- Proteomic analysis of the liver regulating lipid metabolism in Chaohu ducks using two-dimensional electrophoresis
- Nasopharyngeal tuberculosis: A case report
- Characterization and evaluation of anti-Salmonella enteritidis activity of indigenous probiotic lactobacilli in mice
- Aberrant pulmonary immune response of obese mice to periodontal infection
- Bacteriospermia – A formidable player in male subfertility
- In silico and in vivo analysis of TIPE1 expression in diffuse large B cell lymphoma
- Effects of KCa channels on biological behavior of trophoblasts
- Interleukin-17A influences the vulnerability rather than the size of established atherosclerotic plaques in apolipoprotein E-deficient mice
- Multiple organ failure and death caused by Staphylococcus aureus hip infection: A case report
- Prognostic signature related to the immune environment of oral squamous cell carcinoma
- Primary and metastatic squamous cell carcinoma of the thyroid gland: Two case reports
- Neuroprotective effects of crocin and crocin-loaded niosomes against the paraquat-induced oxidative brain damage in rats
- Role of MMP-2 and CD147 in kidney fibrosis
- Geometric basis of action potential of skeletal muscle cells and neurons
- Babesia microti-induced fulminant sepsis in an immunocompromised host: A case report and the case-specific literature review
- Role of cerebellar cortex in associative learning and memory in guinea pigs
- Application of metagenomic next-generation sequencing technique for diagnosing a specific case of necrotizing meningoencephalitis caused by human herpesvirus 2
- Case report: Quadruple primary malignant neoplasms including esophageal, ureteral, and lung in an elderly male
- Long non-coding RNA NEAT1 promotes angiogenesis in hepatoma carcinoma via the miR-125a-5p/VEGF pathway
- Osteogenic differentiation of periodontal membrane stem cells in inflammatory environments
- Knockdown of SHMT2 enhances the sensitivity of gastric cancer cells to radiotherapy through the Wnt/β-catenin pathway
- Continuous renal replacement therapy combined with double filtration plasmapheresis in the treatment of severe lupus complicated by serious bacterial infections in children: A case report
- Simultaneous triple primary malignancies, including bladder cancer, lymphoma, and lung cancer, in an elderly male: A case report
- Preclinical immunogenicity assessment of a cell-based inactivated whole-virion H5N1 influenza vaccine
- One case of iodine-125 therapy – A new minimally invasive treatment of intrahepatic cholangiocarcinoma
- S1P promotes corneal trigeminal neuron differentiation and corneal nerve repair via upregulating nerve growth factor expression in a mouse model
- Early cancer detection by a targeted methylation assay of circulating tumor DNA in plasma
- Calcifying nanoparticles initiate the calcification process of mesenchymal stem cells in vitro through the activation of the TGF-β1/Smad signaling pathway and promote the decay of echinococcosis
- Evaluation of prognostic markers in patients infected with SARS-CoV-2
- N6-Methyladenosine-related alternative splicing events play a role in bladder cancer
- Characterization of the structural, oxidative, and immunological features of testis tissue from Zucker diabetic fatty rats
- Effects of glucose and osmotic pressure on the proliferation and cell cycle of human chorionic trophoblast cells
- Investigation of genotype diversity of 7,804 norovirus sequences in humans and animals of China
- Characteristics and karyotype analysis of a patient with turner syndrome complicated with multiple-site tumors: A case report
- Aggravated renal fibrosis is positively associated with the activation of HMGB1-TLR2/4 signaling in STZ-induced diabetic mice
- Distribution characteristics of SARS-CoV-2 IgM/IgG in false-positive results detected by chemiluminescent immunoassay
- SRPX2 attenuated oxygen–glucose deprivation and reperfusion-induced injury in cardiomyocytes via alleviating endoplasmic reticulum stress-induced apoptosis through targeting PI3K/Akt/mTOR axis
- Aquaporin-8 overexpression is involved in vascular structure and function changes in placentas of gestational diabetes mellitus patients
- Relationship between CRP gene polymorphisms and ischemic stroke risk: A systematic review and meta-analysis
- Effects of growth hormone on lipid metabolism and sexual development in pubertal obese male rats
- Cloning and identification of the CTLA-4IgV gene and functional application of vaccine in Xinjiang sheep
- Antitumor activity of RUNX3: Upregulation of E-cadherin and downregulation of the epithelial–mesenchymal transition in clear-cell renal cell carcinoma
- PHF8 promotes osteogenic differentiation of BMSCs in old rat with osteoporosis by regulating Wnt/β-catenin pathway
- A review of the current state of the computer-aided diagnosis (CAD) systems for breast cancer diagnosis
- Bilateral dacryoadenitis in adult-onset Still’s disease: A case report
- A novel association between Bmi-1 protein expression and the SUVmax obtained by 18F-FDG PET/CT in patients with gastric adenocarcinoma
- The role of erythrocytes and erythroid progenitor cells in tumors
- Relationship between platelet activation markers and spontaneous abortion: A meta-analysis
- Abnormal methylation caused by folic acid deficiency in neural tube defects
- Silencing TLR4 using an ultrasound-targeted microbubble destruction-based shRNA system reduces ischemia-induced seizures in hyperglycemic rats
- Plant Sciences
- Seasonal succession of bacterial communities in cultured Caulerpa lentillifera detected by high-throughput sequencing
- Cloning and prokaryotic expression of WRKY48 from Caragana intermedia
- Novel Brassica hybrids with different resistance to Leptosphaeria maculans reveal unbalanced rDNA signal patterns
- Application of exogenous auxin and gibberellin regulates the bolting of lettuce (Lactuca sativa L.)
- Phytoremediation of pollutants from wastewater: A concise review
- Genome-wide identification and characterization of NBS-encoding genes in the sweet potato wild ancestor Ipomoea trifida (H.B.K.)
- Alleviative effects of magnetic Fe3O4 nanoparticles on the physiological toxicity of 3-nitrophenol to rice (Oryza sativa L.) seedlings
- Selection and functional identification of Dof genes expressed in response to nitrogen in Populus simonii × Populus nigra
- Study on pecan seed germination influenced by seed endocarp
- Identification of active compounds in Ophiopogonis Radix from different geographical origins by UPLC-Q/TOF-MS combined with GC-MS approaches
- The entire chloroplast genome sequence of Asparagus cochinchinensis and genetic comparison to Asparagus species
- Genome-wide identification of MAPK family genes and their response to abiotic stresses in tea plant (Camellia sinensis)
- Selection and validation of reference genes for RT-qPCR analysis of different organs at various development stages in Caragana intermedia
- Cloning and expression analysis of SERK1 gene in Diospyros lotus
- Integrated metabolomic and transcriptomic profiling revealed coping mechanisms of the edible and medicinal homologous plant Plantago asiatica L. cadmium resistance
- A missense variant in NCF1 is associated with susceptibility to unexplained recurrent spontaneous abortion
- Assessment of drought tolerance indices in faba bean genotypes under different irrigation regimes
- The entire chloroplast genome sequence of Asparagus setaceus (Kunth) Jessop: Genome structure, gene composition, and phylogenetic analysis in Asparagaceae
- Food Science
- Dietary food additive monosodium glutamate with or without high-lipid diet induces spleen anomaly: A mechanistic approach on rat model
- Binge eating disorder during COVID-19
- Potential of honey against the onset of autoimmune diabetes and its associated nephropathy, pancreatitis, and retinopathy in type 1 diabetic animal model
- FTO gene expression in diet-induced obesity is downregulated by Solanum fruit supplementation
- Physical activity enhances fecal lactobacilli in rats chronically drinking sweetened cola beverage
- Supercritical CO2 extraction, chemical composition, and antioxidant effects of Coreopsis tinctoria Nutt. oleoresin
- Functional constituents of plant-based foods boost immunity against acute and chronic disorders
- Effect of selenium and methods of protein extraction on the proteomic profile of Saccharomyces yeast
- Microbial diversity of milk ghee in southern Gansu and its effect on the formation of ghee flavor compounds
- Ecology and Environmental Sciences
- Effects of heavy metals on bacterial community surrounding Bijiashan mining area located in northwest China
- Microorganism community composition analysis coupling with 15N tracer experiments reveals the nitrification rate and N2O emissions in low pH soils in Southern China
- Genetic diversity and population structure of Cinnamomum balansae Lecomte inferred by microsatellites
- Preliminary screening of microplastic contamination in different marine fish species of Taif market, Saudi Arabia
- Plant volatile organic compounds attractive to Lygus pratensis
- Effects of organic materials on soil bacterial community structure in long-term continuous cropping of tomato in greenhouse
- Effects of soil treated fungicide fluopimomide on tomato (Solanum lycopersicum L.) disease control and plant growth
- Prevalence of Yersinia pestis among rodents captured in a semi-arid tropical ecosystem of south-western Zimbabwe
- Effects of irrigation and nitrogen fertilization on mitigating salt-induced Na+ toxicity and sustaining sea rice growth
- Bioengineering and Biotechnology
- Poly-l-lysine-caused cell adhesion induces pyroptosis in THP-1 monocytes
- Development of alkaline phosphatase-scFv and its use for one-step enzyme-linked immunosorbent assay for His-tagged protein detection
- Development and validation of a predictive model for immune-related genes in patients with tongue squamous cell carcinoma
- Agriculture
- Effects of chemical-based fertilizer replacement with biochar-based fertilizer on albic soil nutrient content and maize yield
- Genome-wide identification and expression analysis of CPP-like gene family in Triticum aestivum L. under different hormone and stress conditions
- Agronomic and economic performance of mung bean (Vigna radiata L.) varieties in response to rates of blended NPS fertilizer in Kindo Koysha district, Southern Ethiopia
- Influence of furrow irrigation regime on the yield and water consumption indicators of winter wheat based on a multi-level fuzzy comprehensive evaluation
- Discovery of exercise-related genes and pathway analysis based on comparative genomes of Mongolian originated Abaga and Wushen horse
- Lessons from integrated seasonal forecast-crop modelling in Africa: A systematic review
- Evolution trend of soil fertility in tobacco-planting area of Chenzhou, Hunan Province, China
- Animal Sciences
- Morphological and molecular characterization of Tatera indica Hardwicke 1807 (Rodentia: Muridae) from Pothwar, Pakistan
- Research on meat quality of Qianhua Mutton Merino sheep and Small-tail Han sheep
- SI: A Scientific Memoir
- Suggestions on leading an academic research laboratory group
- My scientific genealogy and the Toronto ACDC Laboratory, 1988–2022
- Erratum
- Erratum to “Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study”
- Erratum to “A two-microRNA signature predicts the progression of male thyroid cancer”
- Retraction
- Retraction of “Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis”