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Variations in the bacterial and fungal community structure along the hypoxic gradient of the Arabian Sea oxygen-depleted environment based on eDNA metabarcoding analysis

  • Vilas Bhagwat Phartade

    Dr. Vilas Bhagwat Phartade is a researcher in the Biological Oceanography Division at CSIR-National Institute of Oceanography, Goa, India. He recently completed his Ph.D. in Biotechnology, where he investigated the beneficial properties of coral mucus and its associated microbial communities, focusing on their roles in coral health under diverse environmental conditions. Following this, he expanded his research to include the characterization of microbial communities across various marine habitats.

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    , Ashutosh Shankar Parab

    Dr. Ashutosh Shankar Parab, senior project associate, is a marine microbiologist specializing in microbial ecology and biogeochemical cycling within marine ecosystems including oxygen minimum zones. His research mainly integrates metagenomics, and functional profiling through molecular tools to explore microbial diversity and carbon dynamics across marine environments.

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    , Cathrine Sumathi Manohar

    Dr. Cathrine Sumathi Manohar is a senior principal scientist with 20 years of research experience in various aspects of Marine Sciences especially in Microbiology, Molecular Biology, Biotechnology and Biological Oceanography. Research work mainly deals with understanding microbial diversity using molecular techniques. She has studied the biotechnological potential of mangrove, seaweed and coral-associated microbes. She has successfully led and been a team member in over 10 research projects, funded by various ministries from the Government of India.

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    , Pravin Kumar

    Dr. Pravin Kumar is a research fellow under the supervision of Dr. S. Krishnamurthi at MTCC, CSIR-IMTECH, Chandigarh, India. His work focuses on exploring the biopotentials of marine prokaryotes, particularly their interactions with algae, corals, and sponges.

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    and Srinivasan Krishnamurthi

    Dr. Srinivasan Krishnamurthi is a principal scientist at the Microbial Type Culture Collection and Gene Bank (MTCC), CSIR-Institute of Microbial Technology (CSIR-IMTECH), Chandigarh, India. His research group focuses on exploring the diversity of extremophiles, rare or difficult-to-cultivate prokaryotic communities, and host-associated microbes, with an emphasis on their ecological significance and bioprospecting potential.

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Published/Copyright: May 1, 2025

Abstract

The Arabian Sea hosts one of the major perennial, oceanic oxygen-depleted environments (ODE) in the water column, influencing the seabed beneath it. These regions harbor a vast diversity of microbial communities, which play a significant role in the global budgets of key biogenic elements like carbon, nitrogen and oxygen. This study assessed the relative importance of bacterial and fungal communities in the Arabian Sea ODE using eDNA metabarcoding tools. Sediment samples from four stations at ∼200–1,200 m depths were analyzed across a hypoxic gradient, with 5–35 μM dissolved oxygen levels. Species diversity and richness indices revealed that bacterial and fungal communities were the highest at an oxygen threshold of 10–20 μM, with variations in their community composition along the hypoxic gradient. The bacterial phylum Proteobacteria was dominant in the sediment of all stations. However, the relative abundances of phyla such as Firmicutes, Chloroflexi, Bacteroidetes, Planctomycetes and Actinobacteria varied across the stations. The phyla Ascomycota and Basidiomycota dominated the fungal communities at all the stations. However, Mucoromycota was present only at stations with 20–35 μM oxygen levels. These results enhance our understanding of microbial community distribution in the Arabian Sea ODE.


Corresponding author: Cathrine Sumathi Manohar, Biological Oceanography Division, CSIR-National Institute of Oceanography, Dona Paula, Goa, India; and Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, Uttar Pradesh, India, E-mail:
Vilas Bhagwat Phartade and Ashutosh Shankar Parab contributed equally to this work.

Award Identifier / Grant number: PSC0108

About the authors

Vilas Bhagwat Phartade

Dr. Vilas Bhagwat Phartade is a researcher in the Biological Oceanography Division at CSIR-National Institute of Oceanography, Goa, India. He recently completed his Ph.D. in Biotechnology, where he investigated the beneficial properties of coral mucus and its associated microbial communities, focusing on their roles in coral health under diverse environmental conditions. Following this, he expanded his research to include the characterization of microbial communities across various marine habitats.

Ashutosh Shankar Parab

Dr. Ashutosh Shankar Parab, senior project associate, is a marine microbiologist specializing in microbial ecology and biogeochemical cycling within marine ecosystems including oxygen minimum zones. His research mainly integrates metagenomics, and functional profiling through molecular tools to explore microbial diversity and carbon dynamics across marine environments.

Cathrine Sumathi Manohar

Dr. Cathrine Sumathi Manohar is a senior principal scientist with 20 years of research experience in various aspects of Marine Sciences especially in Microbiology, Molecular Biology, Biotechnology and Biological Oceanography. Research work mainly deals with understanding microbial diversity using molecular techniques. She has studied the biotechnological potential of mangrove, seaweed and coral-associated microbes. She has successfully led and been a team member in over 10 research projects, funded by various ministries from the Government of India.

Pravin Kumar

Dr. Pravin Kumar is a research fellow under the supervision of Dr. S. Krishnamurthi at MTCC, CSIR-IMTECH, Chandigarh, India. His work focuses on exploring the biopotentials of marine prokaryotes, particularly their interactions with algae, corals, and sponges.

Srinivasan Krishnamurthi

Dr. Srinivasan Krishnamurthi is a principal scientist at the Microbial Type Culture Collection and Gene Bank (MTCC), CSIR-Institute of Microbial Technology (CSIR-IMTECH), Chandigarh, India. His research group focuses on exploring the diversity of extremophiles, rare or difficult-to-cultivate prokaryotic communities, and host-associated microbes, with an emphasis on their ecological significance and bioprospecting potential.

Acknowledgments

The authors are thankful to the captain, crew, ship cell staff and colleagues on board RV Sindhu Sankalp for all their support during cruise no. SSK046. They are also thankful for Research Grant no. PSC0108 from the Council of Scientific and Industrial Research, India. This is NIO manuscript contribution no. 7409.

  1. Research ethics: This article contains no animal studies and meets the ethical guidelines.

  2. Informed consent: Not applicable.

  3. Author contributions: Phartade Vilas Bhagwat and Ashutosh Shankar Parab was responsible for the data curation, writing and editing of the manuscript. Cathrine Sumathi Manohar was responsible for the conceptualisation, fund acquisition, data curation, provided supervision, manuscript preparation, review and editing. Pravin Kumar contributed in the data analysis, validation and preparation of the manuscript. Srinivasan Krishnamurthi contributed to the data analysis, review and editing. The authors have accepted responsibility for the entire content of this manuscript and approved its submission.

  4. Use of Large Language Models, AI and Machine Learning Tools: None declared.

  5. Conflict of interest: The authors state no conflict of interest.

  6. Research funding: This study was supported by the research project INDIAS IDEA: Indian Aquatic Ecosystems: Impact of Deoxygenation, Eutrophication and Acidification (Grant no. PSC0108) from Council of Scientific and Industrial Research, India.

  7. Data availability: Metagenomic data used for this manuscript is deposited in the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) under the bio project identifier PRJNA1060920.

References

Amberkar, U., Khandeparker, R.D., Menezes, L., and Meena, R.M. (2021). Phylogenetic diversity of culturable marine bacteria from sediments underlying the oxygen minimum zone of the Arabian Sea and their role in nitrate reduction. Mar. Ecol. 42: 12646, https://doi.org/10.1111/maec.12646.Search in Google Scholar

Andrews, S. (2010). FastQC. A quality control tool for high throughput sequence data, https://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (Accessed 28 February 2024).Search in Google Scholar

Bandekar, M., Ramaiah, N., and Meena, R.M. (2018). Diversity and abundance of denitrifying and anammox bacteria from the Arabian Sea oxygen minimum zone. Deep Sea Res. II: Top. Stud. Oceanogr. 156: 19–26, https://doi.org/10.1016/j.dsr2.2018.08.008.Search in Google Scholar

Bange, H.W., Naqvi, S.W.A., and Codispoti, L.A. (2005). The nitrogen cycle in the Arabian Sea. Prog. Oceanogr. 65: 145–158, https://doi.org/10.1016/j.pocean.2005.03.002.Search in Google Scholar

Barnes, N.M., Damare, S.R., and Shenoy, B.D. (2021). Bacterial and fungal diversity in sediment and water column from the abyssal regions of the Indian Ocean. Front. Mar. Sci. 8: 687860, https://doi.org/10.3389/fmars.2021.687860.Search in Google Scholar

Bertagnolli, A.D. and Stewart, F.J. (2018). Microbial niches in marine oxygen minimum zones. Nat. Revi. Micro. 16: 723–729, https://doi.org/10.1038/s41579-018-0087-z.Search in Google Scholar PubMed

Bhattacharya, S., Mapder, T., Fernandes, S., Roy, C., Sarkar, J., Rameez, M.J., Ghosh, W., Sar, A., Chakraborty, A.K., Mondal, N., et al.. (2021). Sedimentation rate and organic matter dynamics shape microbiomes across a continental margin. Biogeosciences 18: 5203–5222, https://doi.org/10.5194/bg-18-5203-2021.Search in Google Scholar

Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., et al.. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7: 335–336, https://doi.org/10.1038/nmeth.f.303.Search in Google Scholar PubMed PubMed Central

Chen, Q., Tang, K., Chen, X., and Jiao, N. (2022). Microbial sulfurization stimulates carbon sequestration in marine oxygen minimum zones. Sci. Bull. 67: 895–898, https://doi.org/10.1016/j.scib.2022.01.028.Search in Google Scholar PubMed

Divya, B., Soumya, K.V., and Nair, S. (2010). 16S rRNA and enzymatic diversity of culturable bacteria from the sediments of oxygen minimum zone in the Arabian Sea. Antonie van Leeuwenhoek 98: 9–18, https://doi.org/10.1007/s10482-010-9423-7.Search in Google Scholar PubMed

Divya, B., Parvathi, A., Bharathi, P.L., and Nair, S. (2011). 16S rRNA-based bacterial diversity in the organic rich sediments underlying oxygen-deficient waters of the eastern Arabian Sea. World J. Microbiol. Biotechnol. 27: 2821–2833, https://doi.org/10.1007/s11274-011-0760-0.Search in Google Scholar

Engel, A., Kiko, R., and Dengler, M. (2022). Organic matter supply and utilization in oxygen minimum zones. Ann. Rev. Mar. Sci. 14: 355–378, https://doi.org/10.1146/annurev-marine-041921-090849.Search in Google Scholar PubMed

Fenchel, T. and Finlay, B. (2008). Oxygen and the spatial structure of microbial communities. Biol. Rev. 83: 553–569, https://doi.org/10.1111/j.1469-185x.2008.00054.x.Search in Google Scholar PubMed

Fernandes, G.L., Shenoy, B.D., Menezes, L.D., Meena, R.M., and Damare, S.R. (2019). Prokaryotic diversity in oxygen depleted waters of the Bay of Bengal inferred using culture dependent and independent methods. Ind. J. Microbiol. 59: 193–199, https://doi.org/10.1007/s12088-019-00786-1.Search in Google Scholar PubMed PubMed Central

Fernandes, G.L., Shenoy, B.D., and Damare, S.R. (2020). Diversity of bacterial community in the oxygen minimum zones of Arabian Sea and Bay of Bengal as deduced by Illumina sequencing. Front. Microbiol. 10: 481205, https://doi.org/10.3389/fmicb.2019.03153.Search in Google Scholar PubMed PubMed Central

Fuchsman, C.A., Cherubini, L., and Hays, M.D. (2022). An analysis of protists in Pacific oxygen deficient zones: implications for Prochlorococcus and N2‐producing bacteria. Environ. Microbiol. 24: 1790–1804, https://doi.org/10.1111/1462-2920.15893.Search in Google Scholar PubMed

Gardes, M. and Bruns, T.D. (1993). ITS primers with enhanced specificity for basidiomycetes– application to the identification of mycorrhizae and rusts. Mol. Ecol. 2: 113–118, https://doi.org/10.1111/j.1365-294x.1993.tb00005.x.Search in Google Scholar PubMed

Guo, X., Song, G., Li, Y., Zhao, L., and Wang, J. (2022). Switch of bacteria community under oxygen depletion in sediment of Bohai Sea. Front. Mar. Sci. 9: 833513, https://doi.org/10.3389/fmars.2022.833513.Search in Google Scholar

Hammer, O., Harper, D.A., and Ryan, P.D. (2001). Palaeontological statistics software package for education and data analysis. Palaeontol. Electron. 4: 1–9.Search in Google Scholar

Helly, J.J. and Levin, L.A. (2004). Global distribution of naturally occurring marine hypoxia on margins. Deep Sea Res Part I: Oceangr. Res. Pap. 51: 1159–1168, https://doi.org/10.1016/j.dsr.2004.03.009.Search in Google Scholar

Isaacs, M.J., Ramadoss, D., Parab, A.S., and Manohar, C.S. (2021). Evaluating the bacterial diversity from the southwest coast of India using fatty acid methyl ester profiles. Curr. Microbiol. 78: 649–658, https://doi.org/10.1007/s00284-020-02315-6.Search in Google Scholar PubMed

Jasmin, C., Anas, A., Tharakan, B., Jaleel, A., Puthiyaveettil, V., Narayanan, S., Lincy, J., and Nair, S. (2017). Diversity of sediment‐associated Planctomycetes in the Arabian Sea oxygen minimum zone. J. Basic Microbiol. 57: 1010–1017, https://doi.org/10.1002/jobm.201600750.Search in Google Scholar PubMed

Jayakumar, A., O’mullan, G.D., Naqvi, S.W.A., and Ward, B.B. (2009). Denitrifying bacterial composition changes associated with stages of denitrification in oxygen minimum zones. Microb. Ecol. 58: 350–362, https://doi.org/10.1007/s00248-009-9487-y.Search in Google Scholar PubMed

Jayakumar, A., Peng, X., and Ward, B.B. (2013). Community composition of bacteria involved in fixed nitrogen loss in the water column of two major oxygen minimum zones in the ocean. Aquat. Microb. Ecol. 70: 245–259, https://doi.org/10.3354/ame01654.Search in Google Scholar

Jebaraj, C.S. and Raghukumar, C. (2009). Anaerobic denitrification in fungi from the coastal marine sediments off Goa, India. Mycol. Res. 113: 100–109, https://doi.org/10.1016/j.mycres.2008.08.009.Search in Google Scholar PubMed

Jebaraj, C.S. and Raghukumar, C. (2010). Nitrate reduction by fungi in marine oxygen-depleted laboratory microcosms. Bot. Mar. 53: 469–474, https://doi.org/10.1515/bot.2010.046.Search in Google Scholar

Jebaraj, C.S., Raghukumar, C., Behnke, A., and Stoeck, T. (2010). Fungal diversity in oxygen depleted regions of the Arabian Sea revealed by targeted environmental sequencing combined with cultivation. FEMS Microbiol. Ecol. 71: 399–412, https://doi.org/10.1111/j.1574-6941.2009.00804.x.Search in Google Scholar PubMed

Kurakov, A.V., Lavrent’ev, R.B., Nechitailo, T.Yu., Golyshin, P.N., and Zvyagintsev, D.G. (2008). Diversity of facultatively anaerobic microscopic mycelial fungi in soils. Microbiology 77: 90–98, https://doi.org/10.1134/s002626170801013x.Search in Google Scholar

Lam, P. and Kuypers, M.M. (2011). Microbial nitrogen cycling processes in oxygen minimum zones. Ann. Rev. Mar. Sci. 3: 317–345, https://doi.org/10.1146/annurev-marine-120709-142814.Search in Google Scholar PubMed

Laughlin, R.J., Rütting, T., Müller, C., Watson, C.J., and Stevens, R.J. (2009). Effect of acetate on soil respiration, N2O emissions and gross N transformations related to fungi and bacteria in a grassland soil. Appl. Soil Ecol. 42: 25–30.10.1016/j.apsoil.2009.01.004Search in Google Scholar

Li, D., Wang, L., Jiang, F., Zeng, X., Xu, Q., Zhang, X., Zheng, Q., and Shao, Z. (2024). Prokaryotic community structure and key taxa in the Arabian Sea’s oxygen minimum zone. Front. Mar. Sci. 11: 138–0819, https://doi.org/10.3389/fmars.2024.1380819.Search in Google Scholar

Lincy, J. and Manohar, C.S. (2020). A comparison of bacterial communities from OMZ sediments in the Arabian Sea and the Bay of Bengal reveals major differences in nitrogen turnover and carbon recycling potential. Mar. Biol. Res. 16: 656–673, https://doi.org/10.1080/17451000.2020.1840593.Search in Google Scholar

Lincy, J. and Manohar, C.S. (2021). 16S rRNA and hydrazine gene-based profiling of the Candidatus scalindua community from the Arabian Sea hypoxic sediment. Curr. Sci. 120: 684–693, https://doi.org/10.18520/cs/v120/i4/684-693.Search in Google Scholar

Long, A.M., Jurgensen, S.K., Petchel, A.R., Savoie, E.R., and Brum, J.R. (2021). Microbial ecology of oxygen minimum zones amidst ocean deoxygenation. Front. Microbiol. 12: 748961, https://doi.org/10.3389/fmicb.2021.748961.Search in Google Scholar PubMed PubMed Central

Manohar, C.S. and Raghukumar, C. (2013). Fungal diversity from various marine habitats deduced through culture independent studies. FEMS Microbiol. Lett. 341: 69–78, https://doi.org/10.1111/1574-6968.12087.Search in Google Scholar PubMed

Manohar, C.S., Menezes, L.D., Ramasamy, K.P., and Meena, R.M. (2015). Phylogenetic analyses and nitrate reducing activity of fungal cultures isolated from the permanent, oceanic oxygen minimum zone of the Arabian Sea. Can. J. Microbiol. 61: 217–226, https://doi.org/10.1139/cjm-2014-0507.Search in Google Scholar PubMed

McMurdie, P.J. and Holmes, S. (2013). phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PloS One 8: 61217, https://doi.org/10.1371/journal.pone.0061217.Search in Google Scholar PubMed PubMed Central

Mulla, A., Fernandes, G., Menezes, L., Meena, R.M., Naik, H., Gauns, M., and Damare, S. (2018). Diversity of culturable nitrate-reducing bacteria from the Arabian Sea oxygen minimum zone. Deep-Sea Res. II: Top. Stud. Oceanogr. 156: 27–33, https://doi.org/10.1016/j.dsr2.2017.12.014.Search in Google Scholar

Muyzer, G., de Waal, E.C., and Uitterlinden, A.G. (1993). Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction–amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59: 695–700, https://doi.org/10.1128/aem.59.3.695-700.1993.Search in Google Scholar PubMed PubMed Central

Naqvi, S.W.A., Jayakumar, D.A., Narvekar, P.V., Naik, H., Sarma, V.V.S.S., D’Souza, W., and George, M.D. (2000). Increased marine production of N2O due to intensifying anoxia on the Indian continental shelf. Nature 408: 346–349, https://doi.org/10.1038/35042551.Search in Google Scholar PubMed

Naqvi, S.W.A., Naik, H., Pratihary, A., D’souza, W., Narvekar, P.V., Jayakumar, D.A., Devol, A.H., Yoshinari, T., and Saino, T. (2006). Coastal versus open–ocean denitrification in the Arabian Sea. Biogeosciences 3: 621–633, https://doi.org/10.5194/bg-3-621-2006.Search in Google Scholar

Nguyen, N.P., Warnow, T., Pop, M., and White, B. (2016). A perspective on 16S rRNA operational taxonomic unit clustering using sequence similarity. NPJ Biofilms Microbiomes 2: 1–8, https://doi.org/10.1038/npjbiofilms.2016.4.Search in Google Scholar PubMed PubMed Central

Pan, H., Qin, Y., Wang, Y., Liu, S., Yu, B., Song, Y., Wang, X., and Zhu, G. (2020). Dissimilatory nitrate/nitrite reduction to ammonium (DNRA) pathway dominates nitrate reduction processes in rhizosphere and non-rhizosphere of four fertilized farmland soil. Environ. Res. 186: 109612, https://doi.org/10.1016/j.envres.2020.109612.Search in Google Scholar PubMed

Parab, A.S. and Manohar, C.S. (2024). Insights into the seasonal changes in the taxonomic and functional diversity of bacteria in the eastern Arabian Sea: shotgun metagenomics approach. Mar. Environ. Res. 199: 106616, https://doi.org/10.1016/j.marenvres.2024.106616.Search in Google Scholar PubMed

Parab, A.S. and Manohar, C.S. (2025). Bacterial dynamics in the northern Indian Ocean region: understanding from the pre–genomics to present–day OMICS era. Geomicrobiol. J. 42: 113–124, https://doi.org/10.1080/01490451.2024.2437462.Search in Google Scholar

Parab, A.S., Jagtap, A.S., Meena, R.M., and Manohar, C.S. (2022). Bacterial dynamics along the west coast of India during the non–monsoon and monsoon season. Cont. Shelf Res. 251: 104876, https://doi.org/10.1016/j.csr.2022.104876.Search in Google Scholar

Parab, A.S., Ghose, M., Manohar, C.S., Gauns, M.U., and Paul, S. (2024). Metagenomic insights into bacterial dynamics and niche partitioning in response to varying oxygen gradients in the Arabian Sea oxygen minimum zone (OMZ). Reg. Stud. Mar. Sci. 78: 103768, https://doi.org/10.1016/j.rsma.2024.103768.Search in Google Scholar

Posadas, J., Velez, P., Pajares, S., Gasca–Pineda, J., and Espinosa–Asuar, L. (2024). Fungal diversity in sediments of the eastern tropical Pacific oxygen minimum zone revealed by metabarcoding. PloS One 19: 0301605, https://doi.org/10.1371/journal.pone.0301605.Search in Google Scholar PubMed PubMed Central

Rixen, T., Cowie, G., Gaye, B., Goes, J., Do Rosário Gomes, H., Hood, R.R., Lachkar, Z., Schmidt, H., Segschneider, J., and Singh, A. (2020). Reviews and syntheses: present, past and future of the oxygen minimum zone in the northern Indian Ocean. Biogeosciences 17: 6051–6080, https://doi.org/10.5194/bg-17-6051-2020.Search in Google Scholar

Singh, P., Raghukumar, C., Pankaj, V., and Yogesh, S. (2011). Fungal community analysis in the deep–sea sediments of the Central Indian basin by culture–independent approach. Microb. Ecol. 61: 507–517, https://doi.org/10.1007/s00248-010-9765-8.Search in Google Scholar PubMed

Spatafora, J.W., Chang, Y., Benny, G.L., Lazarus, K., Smith, M.E., Berbee, M.L., Bonito, G., Corradi, N., Grigoriev, I., Gryganskyi, A., et al.. (2016). A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108: 1028–1046, https://doi.org/10.3852/16-042.Search in Google Scholar PubMed PubMed Central

Spietz, R.L., Williams, C.M., Rocap, G., and Horner–Devine, M.C. (2015). A dissolved oxygen threshold for shifts in bacterial community structure in a seasonally hypoxic estuary. PloS One 10: 0135731, https://doi.org/10.1371/journal.pone.0135731.Search in Google Scholar PubMed PubMed Central

Stief, P., Fuchs-Ocklenburg, S., Kamp, A., Manohar, C.-S., Houbraken, J., Boekhout, T., De Beer, D., and Stoeck, T. (2014). Dissimilatory nitrate reduction by Aspergillus terreus isolated from the seasonal oxygen minimum zone in the Arabian Sea. BMC Microbiol. 14: 1–10, https://doi.org/10.1186/1471-2180-14-35.Search in Google Scholar PubMed PubMed Central

Sun, K., Yu, M., Zhu, X.-Y., Xue, C.-X., Zhang, Y., Chen, X., Yao, P., Chen, L., Fu, L., Yang, Z., et al. (2023). Microbial communities related to the sulfur cycle in the Sansha Yongle Blue Hole. Microbiol. Spectr. 11, https://doi.org/10.1128/spectrum.01149-23.Search in Google Scholar PubMed PubMed Central

Tsai, Y.L. and Olson, B.H. (1991). Rapid method for direct extraction of DNA from soil and sediments. Appl. Environ. Microbiol. 57: 1070–1074, https://doi.org/10.1128/aem.57.4.1070-1074.1991.Search in Google Scholar PubMed PubMed Central

Villanueva, L., Speth, D.R., Van Alen, T., Hoischen, A., and Jetten, M.S.M. (2014). Shotgun metagenomic data reveals significant abundance but low diversity of Candidatus Scalindua marine anammox bacteria in the Arabian Sea oxygen minimum zone. Front. Microbiol. 5: 1–9, https://doi.org/10.3389/fmicb.2014.00031.Search in Google Scholar PubMed PubMed Central

Vuillemin, A. (2023). Nitrogen cycling activities during decreased stratification in the coastal oxygen minimum zone off Namibia. Front. Microbiol. 14: 1101902, https://doi.org/10.3389/fmicb.2023.1101902.Search in Google Scholar PubMed PubMed Central

Vossenberg, V.D.J., Woebken, D., Maalcke, W.J., Wessels, H.J.C.T., Dutilh, B.E., Kartal, B., Janssen‐Megens, E.M., Roeselers, G., Yan, J., Speth, D., et al.. (2013). The metagenome of the marine anammox bacterium Candidatus scalindua profunda illustrates the versatility of this globally important nitrogen cycle bacterium. Environ. Microbiol. 15: 1275–1289, https://doi.org/10.1111/j.1462-2920.2012.02774.x.Search in Google Scholar PubMed PubMed Central

Walters, W., Hyde, E.R., Berg-Lyons, D., Ackermann, G., Humphrey, G., Parada, A., Gilbert, J.A., Jansson, J.K., Caporaso, J.G., Fuhrman, J.A., et al.. (2016). Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems 1: 9–15, https://doi.org/10.1128/msystems.00009-15.Search in Google Scholar

Wang, Y. and Michael, J. (2017). Seasonal cycle of cross‐equatorial flow in the Central Indian Ocean. J. Geophys. Res. Oceans 122: 3817–3827.10.1002/2016JC012537Search in Google Scholar

Ward, B.B., Devol, A.H., Rich, J.J., Chang, B.X., Bulow, S.E., Naik, H., Pratihary, A., and Jayakumar, A. (2009). Denitrification as the dominant nitrogen loss process in the Arabian Sea. Nature 461: 78–81, https://doi.org/10.1038/nature08276.Search in Google Scholar PubMed

Wrighton, K.C., Castelle, C.J., Varaljay, V.A., Satagopan, S., Brown, C.T., Wilkins, M.J., Thomas, B.C., Sharon, I., Williams, K.H., Tabita, F.R., et al.. (2016). RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria. ISME J. 10: 2702–2714, https://doi.org/10.1038/ismej.2016.53.Search in Google Scholar PubMed PubMed Central

Received: 2024-07-03
Accepted: 2025-04-02
Published Online: 2025-05-01
Published in Print: 2025-08-26

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