Influence of ambient geochemical and microbiological variables on the bacterial diversity in a cold seep ecosystem in North Indian Ocean

Abstract

Cold seeps are oases for biological communities on the sea floor around hydrocarbon emission pathways. Microbial utilization of methane and other hydrocarbons yield products that fuel rich chemosynthetic communities at these sites. One such site in the cold seep ecosystem of Krishna-Godavari basin (K-G basin) along the east coast of India, discovered in Feb 2018 at a depth of 1800 m was assessed for its bacterial diversity. The seep bacterial communities were dominated by phylum Proteobacteria (57%), Firmicutes (16%) and unclassified species belonging to the family Helicobacteriaceae. The surface sediments of the seep had maximum OTUs (operational taxonomic units) (2.27 × 10³) with a Shannon alpha diversity index of 8.06. In general, environmental parameters like total organic carbon (p < 0.01), sulfate (p < 0.001), sulfide (p < 0.05) and methane (p < 0.01) were responsible for shaping the bacterial community of the cold seep ecosystem in the K-G Basin. Environmental parameters play a significant role in changing the bacterial diversity richness between different cold seep environments in the oceans.

Keywords

Sediments / Environmental variables / Proteobacteria / Cold seep ecosystem / Organic matter

CRediT authorship contribution statement

Delcy R. Nazareth: Writing – review & editing, Writing – original draft, Visualization, Validation, Software, Methodology, Formal analysis, Data curation. Maria Judith Gonsalves: Writing – review & editing, Writing – original draft, Visualization, Validation, Supervision, Data curation, Conceptualization. Nitisha Sangodkar: Writing – original draft, Visualization, Formal analysis.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

The authors are thankful to the Director, CSIR-NIO for facilities and to VNJCT for funding Ms Nazareth's fellowship. The authors are grateful to the gas hydrate group and the project leader GAP 2303 Dr. A. Mazumdar for the support and cooperation. This is NIO contribution number 7381.

References

E.K. Åström, M.L. Carroll, A. Sen, H. Niemann, W.G. Ambrose Jr, M.F. Lehmann, J. Carroll. Chemosynthesis influences food web and community structure in high-Arctic benthos. Mar. Ecol. Prog. Ser., 629 (2019), pp. 19-42,

E.K. Åström, A. Sen, M.L. Carroll, J. Carroll. Cold Seeps in a warming Arctic: insights for benthic ecology. Front. Mar. Sci., 7 (2020), p. 244,

F. Azam, A.Z. Worden. Microbes, molecules, and marine ecosystems. Science, 303 (5664) (2004), pp. 1622-1624,

D. Bastviken, J. Ejlertsson, L. Tranvik. Measurement of methane oxidation in lakes: a comparison of methods. Environ. Sci. Technol., 36 (15) (2002), pp. 3354-3361,

E. Ben-Dov, E. Kramarsky-Winter, A. Kushmaro. An in situ method for cultivating microorganisms using a double encapsulation technique. FEMS Microbiol. Ecol., 68 (3) (2009), pp. 363-371,

S. Bessette, Y. Moalic, S. Gautey, F. Lesongeur, A. Godfroy, L. Toffin. Relative abundance and diversity of bacterial methanotrophs at the oxic–anoxic interface of the Congo deep-sea fan. Front. Microbiol., 8 (2017), p. 715,

C. Bienhold, P. Pop Ristova, F. Wenzhöfer, T. Dittmar, A. Boetius. How deep-sea wood falls sustain chemosynthetic life. PloS One, 8 (1) (2013), Article e53590,

E.G. Bligh, W.J. Dyer. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol., 37 (8) (1959), pp. 911-917,

A. Boetius, K. Ravenschlag, C.J. Schubert, D. Rickert, F. Widdel, A. Gieseke, et al.. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature, 407 (6804) (2000), pp. 623-626,

Z.F. Burton, L.N. Dafov. Testing the sediment organic contents required for biogenic gas hydrate formation: Insights from synthetic 3-D basin and hydrocarbon system modelling. Fuels, 3 (3) (2022), pp. 555-562,

V. Carrier, M.M. Svenning, F. Gründger, H. Niemann, P.A. Dessandier, G. Panieri, D. Kalenitchenko. The impact of methane on microbial communities at marine arctic gas hydrate bearing sediment. Front. Microbiol., 11 (2020), p. 1932,

D.H. Case, A.L. Pasulka, J.J. Marlow, B.M. Grupe, L.A. Levin, V.J. Orphan. Methane seep carbonates host distinct, diverse, and dynamic microbial assemblages. Mol. Biol. Microbiol., 6 (6) (2015), pp. e01348-e10415,

H. Cho, J.H. Hyun, O.R. You, M. Kim, S.H. Kim, D.L. Choi, et al.. Microbial community structure associated with biogeochemical processes in the sulfate–methane transition zone (SMTZ) of gas-hydrate-bearing sediment of the Ulleung Basin, East Sea. Geomicrobiol. J., 34 (3) (2017), pp. 207-219,

J.D. Cline. Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol. Oceanogr., 14 (3) (1969), pp. 454-458,

M.T. Cottrell, D.L. Kirchman. Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low-and high-molecular-weight dissolved organic matter. Appl. Environ. Microbiol., 66 (4) (2000), pp. 1692-1697,

M.A. Crowe, J.F. Power, X.C. Morgan, P.F. Dunfield, K. Lagutin, W.I.C. Rijpstra, M.B. Stott. Pyrinomonas methylaliphatogenes gen. nov., sp. nov., a novel group 4 thermophilic member of the phylum Acidobacteria from geothermal soils. Int. J. Syst. Evol. Microbiol., 64 (2014), pp. 220-227,

H. Cui, X. Su, F. Chen, M. Holland, S. Yang, J. Liang, W. Hou. Microbial diversity of two cold seep systems in gas hydrate-bearing sediments in the South China Sea. Mar. Environ. Res., 144 (2019), pp. 230-239,

H. Cui, X. Su, J. Liang, F. Chen, M. Holland, S. Yang, H. Dong. Microbial diversity in fracture and pore filling gas hydrate-bearing sediments at Site GMGS2-16 in the Pearl River Mouth Basin, the South China Sea. Mar. Geol., 427 (2020), Article 106264,

X. Dan, S. Liu, X. Feng, L. Lin, R. Tang, C. Yang, et al.. Geochemical record of methane seepage in carbon cycling and possible correlation with climate events in the Qiongdongnan basin, South China Sea. Mar. Petrol. Geol., 149 (2023), Article 106061,

H. Dang, X. Luan, J. Zhao, J. Li. Diverse and novel nifH and nifH-like gene sequences in the deep-sea methane seep sediments of the Okhotsk Sea. Appl. Environ. Microbiol., 75 (7) (2009), pp. 2238-2245,

S.N. Dedysh, P. Yilmaz. Refining the taxonomic structure of the phylum Acidobacteria. Int. J. System. Evolut. Microbiol., 68 (12) (2018), pp. 3796-3806,

de Dios-Cubillas, A., Carrizo, D., Sánchez-García, L., López, I., Prieto-Ballesteros, O., 2021. Biosignatures of Cold Seep Carbonates to Help Understand the Carbon Cycle Within the Ocean Worlds. In: 52nd Lunar and Planetary Science Conference, No. 2548, p. 1446.

A.E. Dekas, R.S. Poretsky, V.J. Orphan. Deep-sea archaea fix and share nitrogen in methane-consuming microbial consortia. Science, 326 (5951) (2009), pp. 422-426,

A.M. Demko, N.V. Patin, P.R. Jensen. Microbial diversity in tropical marine sediments assessed using culture‐dependent and culture‐independent techniques. Environ. Microbiol., 23 (11) (2021), pp. 6859-6875,

P. Dewangan, G. Sriram, A. Kumar, A. Mazumdar, A. Peketi, V. Mahale, A. Babu. Widespread occurrence of methane seeps in deep-water regions of Krishna-Godavari basin, Bay of Bengal. Mar. Petrol. Geol., 124 (2021), Article 104783,

X. Dong, Y. Peng, M. Wang, L. Woods, W. Wu, Y. Wang, C.R. Hubert. Evolutionary ecology of microbial populations inhabiting deep sea sediments associated with cold seeps. Nat. Commun., 14 (1) (2023), p. 1127,

S.K. El Wakeel, J.P. Riley. The determination of organic carbon in marine muds. ICES J. Mar. Sci., 22 (2) (1957), pp. 180-183,

M. Fabiano, R. Danovaro, S. Fraschetti. A three-year time series of elemental and biochemical composition of organic matter in subtidal sandy sediments of the Ligurian Sea (northwestern Mediterranean). Cont. Shelf Res., 15 (1995), p. 1453,

B.Z. Fathepure. Recent studies in microbial degradation of petroleum hydrocarbons in hypersaline environments. Front. Microbiol., 5 (2014), p. 80789,

S.O. Fernandes, M.J. Gonsalves, D.R. Nazareth, S.K. Wong, M.N. Haider, M. Ijichi, K. Kogure. Seasonal variability in environmental parameters influence bacterial communities in mangrove sediments along an estuarine gradient. Estuar. Coast. Shelf Sci., 270 (2022), Article 107791,

R. Fichez. Composition and fate of organic matter in submarine cave sediments; implications for the biogeochemical cycle of organic carbon. Oceanologia Acta, 14 (1991), pp. 369-377

D. Fischer. Cold seeps: marine ecosystems based on hydrocarbons. Science in School, 16 (2010), pp. 60-64

M.J. Gonsalves, C.E. Fernandes, S.O. Fernandes, D.L. Kirchman, P.L. Bharathi. Effects of composition of labile organic matter on biogenic production of methane in the coastal sediments of the Arabian Sea. Environ. Monit. Assess., 182 (2011), pp. 385-395,

S. Grünke, J. Felden, A. Lichtschlag, A.C. Girnth, D. de Beer, F. Wenzhöfer, A. Boetius. Niche differentiation among mat‐forming, sulfide‐oxidizing bacteria at cold seeps of the Nile Deep Sea Fan (Eastern Mediterranean Sea). Geobiology, 9 (4) (2011), pp. 330-348,

S. Guerrero-Cruz, A. Vaksmaa, M.A. Horn, H. Niemann, M. Pijuan, A. Ho. Methanotrophs: discoveries, environmental relevance, and a perspective on current and future applications. Front. Microbiol., 12 (2021), Article 678057,

J.H. Gwak, S.I. Awala, N.L. Nguyen, W.J. Yu, H.Y. Yang, M. von Bergen, S.K. Rhee. Sulfur and methane oxidation by a single microorganism. PNAS, 119 (32) (2022), Article e2114799119,

I.M. Head, D.M. Jones, W.F. Röling. Marine microorganisms make a meal of oil. Nat. Rev. Microbiol., 4 (3) (2006), pp. 173-182,

T. Hoshino, H. Doi, G.I. Uramoto, L. Wörmer, R.R. Adhikari, N. Xiao, et al.. Global diversity of microbial communities in marine sediment. PNAS, 117 (44) (2020), pp. 27587-27597,

L. Jiao, X. Su, Y. Wang, H. Jiang, Y. Zhang, F. Chen. Microbial diversity in the hydrate-containing and-free surface sediments in the Shenhu area, South China Sea. Geosci. Front., 6 (4) (2015), pp. 627-633,

I. Joint, M. Mühling, J. Querellou. Culturing marine bacteria–an essential prerequisite for biodiscovery. Microb. Biotechnol., 3 (5) (2010), pp. 564-575,

T. Katayama, H. Yoshioka, H.A. Takahashi, M. Amo, T. Fujii, S. Sakata. Changes in microbial communities associated with gas hydrates in subseafloor sediments from the Nankai Trough. FEMS Microbiol. Ecol., 92 (8) (2016), Article fiw093,

T. Katayama, H. Yoshioka, M. Kaneko, M. Amo, T. Fujii, H.A. Takahashi, S. Sakata. Cultivation and biogeochemical analyses reveal insights into methanogenesis in deep subseafloor sediment at a biogenic gas hydrate site. ISME J., 16 (5) (2022), pp. 1464-1472,

Kiel S., 2010. The Vent and Seep Biota: Aspects from Microbes to Ecosystems, First ed. Springer Netherlands, 79 pp. https://doi.org/10.1007/978-90-481-9572-5.

N.J. Knab, B.A. Cragg, E.R.C. Hornibrook, L. Holmkvist, R.D. Pancost, C. Borowski, et al.. Regulation of anaerobic methane oxidation in sediments of the Black Sea. Biogeosciences, 6 (8) (2009), pp. 1505-1518,

Kochert, G., 1978. Carbohydrate determination by the phenol-sulfuric acid method. In: Handbook of Phycological Methods: Physiological and Biochemical Methods. Cambridge University Press, Cambridge, UK, pp. 95–97.

M.K. Konopiński. Shannon diversity index: a call to replace the original Shannon’s formula with unbiased estimator in the population genetics studies. PeerJ, 8 (2020), p. e9391

E.H. Lee, K.E. Moon, T.G. Kim, S.D. Lee, K.S. Cho. Inhibitory effects of sulfur compounds on methane oxidation by a methane-oxidizing consortium. J. Biosci. Bioeng., 120 (6) (2015), pp. 670-676,

D.J. Leprich, B.E. Flood, P.R. Schroedl, E. Ricci, J.J. Marlow, P.R. Girguis, J.V. Bailey. Sulfur bacteria promote dissolution of authigenic carbonates at marine methane seeps. ISME J., 15 (7) (2021), pp. 2043-2056,

X. Li, Z. Dai, P. Di, J. Feng, J. Tao, D. Chen, Y. Li. Distinct bottom-water bacterial communities at methane seeps with various seepage intensities in Haima, South China Sea. Front. Mar. Sci., 8 (2021),

H. Li, Y. Lei, T. Li, R. Saraswat. Next-generation sequencing and metabarcoding to understand the ecology of benthic foraminiferal community in the Bering Sea. J. Sea Res., 191 (2023), Article 102321,

J. Liang, J.C. Feng, J. Kong, Y. Huang, H. Zhang, S. Zhong, S. Zhang. Microbial communities and mineral assemblages in sediments from various habitats at the Haima Cold Seep, South China Sea. Front. Mar. Sci., 10 (2023), Article 1254450,

S.J. Lim, L.R. Thompson, C.M. Young, T. Gaasterland, K.D. Goodwin. Dominance of Sulfurospirillum in metagenomes associated with the methane ice worm (Sirsoe methanicola). Appl. Environ. Microbiol., 88 (15) (2022), pp. e00290-e322,

G. Lin, J. Lu, Z. Sun, J. Xie, J. Huang, M. Su, N. Wu. Characterization of tissue-associated bacterial community of two Bathymodiolus species from the adjacent cold seep and hydrothermal vent environments. Sci. Total Environ., 796 (2021), Article 149046,

P.A. Loka Bharathi. The occurrence of denitrifying colourless sulphur-oxidising bacteria in marine waters and sediments as shown by the agar shake technique. FEMS Microbiol. Ecol., 5 (6) (1989), pp. 335-342,

F. Lopes, E. Viollier, A. Thiam, G. Michard, G. Abril, A. Groleau, F. Prevot, D. Jézéquel. Biogeochemical modelling of anaerobic vs. aerobic methane oxidation in a meromictic crater lake (Lake Pavin, France). Appl. Geochem., 26 (12) (2011), pp. 1919-1932,

O.H. Lowry, N.J. Rosebrough, A.L. Farr, R.J. Randall. Protein measurement with the Folin phenol reagent. J. Biol. Chem., 193 (1) (1951), pp. 265-275,

J.B.H. Martiny, B.J. Bohannan, J.H. Brown, R.K. Colwell, J.A. Fuhrman, J.L. Green, J.T. Staley. Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol., 4 (2) (2006), pp. 102-112,

A. Mazumdar, P. Dewangan, A. Peketi, S. Gullapalli, M.S. Kalpana, G.P. Naik, R. Reddy. The first record of active methane (cold) seep ecosystem associated with shallow methane hydrate from the Indian EEZ. J. Earth Syst. Sci., 128 (2019), pp. 1-8,

J. Miyazaki, R. Higa, T. Toki, J. Ashi, U. Tsunogai, T. Nunoura, K. Takai. Molecular characterization of potential nitrogen fixation by anaerobic methane-oxidizing archaea in the methane seep sediments at the number 8 Kumano Knoll in the Kumano Basin, offshore of Japan. Appl. Environ. Microbiol., 75 (22) (2009), pp. 7153-7162,

M.Z. Nawaz, R. Subin Sasidharan, H.A. Alghamdi, H. Dang. Understanding interaction patterns within deep-sea microbial communities and their potential applications. Mar. Drugs, 20 (2) (2022), p. 108,

H. Niemann, P. Linke, K. Knittel, E. MacPherson, A. Boetius, W. Brueckmann, et al.. Methane-carbon flow into the benthic food web at cold seeps–a case study from the Costa Rica subduction zone. PLoS One, 8 (10) (2013), Article e74894,

P. Nimnoi, N. Pongsilp. Marine bacterial communities in the upper gulf of Thailand assessed by Illumina next-generation sequencing platform. BMC MicrobiolM, 20 (2020), pp. 1-11,

P.M. Nguyen. Microbial Sulfur Transformations in Novel Laboratory-Scale Constructed Wetlands Treating Artificial Wastewater. PhD theis, Helmholtz Centre for Environmental Research-UFZ (2016)

D. Oppo, L. De Siena, D.B. Kemp. A record of seafloor methane seepage across the last 150 million years. Sci. Rep., 10 (1) (2020), pp. 1-12,

A.L. Pasulka, L.A. Levin, J.A. Steele, D.H. Case, M.R. Landry, V.J. Orphan. Microbial eukaryotic distributions and diversity patterns in a deep‐sea methane seep ecosystem. Environ. Microbiolm, 18 (9) (2016), pp. 3022-3043,

B.G. Paul, H. Ding, S.C. Bagby, M.Y. Kellermann, M.C. Redmond, G.L. Andersen, D.L. Valentine. Methane-oxidizing bacteria shunt carbon to microbial mats at a marine hydrocarbon seep. Front. Microbiol., 8 (2017), p. 186,

E.T. Peltzer, X. Zhang, P.M. Walz, M. Luna, P.G. Brewer. In situ Raman measurement of HS− and H2S in sediment pore waters and use of the HS−: H2S ratio as an indicator of pore water pH. Mar. Chem., 184 (2016), pp. 32-42,

L.M. Peoples, E. Grammatopoulou, M. Pombrol, X. Xu, O. Osuntokun, J. Blanton, et al.. Microbial community diversity within sediments from two geographically separated hadal trenches. Front. Microbiol., 10 (2019), p. 347,

J.M. Petersen, N. Dubilier. Methanotrophic symbioses in marine invertebrates. Environ. Microbiol. Rep., 1 (5) (2009), pp. 319-335,

A. Pernthaler, A.E. Dekas, C.T. Brown, S.K. Goffredi, T. Embaye, V.J. Orphan. Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics. Proc. Natl. Acad. Sci. U.S.A., 105 (19) (2008), pp. 7052-7057,

P. Pjevac. Co-existence and Niche Differentiation of Sulfur Oxidizing Bacteria in Marine Environments. PhD thesis, University of Bremen Bremen, Germany (2014)

P. Pop Ristova, F. Wenzhöfer, A. Ramette, J. Felden, A. Boetius. Spatial scales of bacterial community diversity at cold seeps (Eastern Mediterranean Sea). ISME J., 9 (6) (2015), pp. 1306-1318,

B. Pontiller, S. Martínez-García, D. Lundin, J. Pinhassi. Labile dissolved organic matter compound characteristics select for divergence in marine bacterial activity and transcription. Front. Microbiol., 11 (2020), Article 588778,

S.S. Qin, M.X. Zhu, Z. Sun, T. Li, X. Zhang, W. Geng, Y. Chen. Diagenetic geochemistry of iron, sulfur, and molybdenum in sediments of the middle Okinawa Trough impacted by hydrothermal plumes and/or cold seeps. Earth Space Sci., 10 (3) (2023), Article e2022EA002709,

P.Y. Qian, Y. Wang, O.O. Lee, S.C. Lau, J. Yang, F.F. Lafi, T.Y. Wong. Vertical stratification of microbial communities in the Red Sea revealed by 16S rDNA pyrosequencing. ISME J., 5 (3) (2011), pp. 507-518,

A.J. Reed, R. Dorn, C.L. Van Dover, R.A. Lutz, C. Vetriani. Phylogenetic diversity of methanogenic, sulfate-reducing and methanotrophic prokaryotes from deep-sea hydrothermal vents and cold seeps. Deep Sea Research Part II: Topical Studies in Oceanography, 56 (19–20) (2009), pp. 1665-1674,

S.E. Ruff, J. Arnds, K. Knittel, R. Amann, G. Wegener, A. Ramette, A. Boetius. Microbial communities of deep-sea methane seeps at Hikurangi continental margin (New Zealand). PloS One, 8 (9) (2013), Article e72627,

L. Russ, B. Kartal, H.J. Op Den Camp, M. Sollai, J. Le Bruchec, J.C. Caprais, et al.. Presence and diversity of anammox bacteria in cold hydrocarbon-rich seeps and hydrothermal vent sediments of the Guaymas Basin. Front. Microbiol., 4 (2013), p. 219,

E.A. Sabu, M.J. Gonsalves, D. Nazareth, R.A. Sreepada. Influence of environmental variables on methane related microbial activities in a tropical bio-secured zero-exchange shrimp culture system. Aquacult. Rep., 22 (2022), Article 100950,

A. Sam Kamaleson, M.J. Gonsalves, D.R. Nazareth. Interactions of sulfur and methane-oxidizing bacteria in tropical estuarine sediments. Environ. Monit. Assess., 191 (2019), pp. 1-18,

N. Sangodkar, M.J. Gonsalves, D.R. Nazareth. Macrofaunal distribution, diversity, and its ecological interaction at the cold seep site of Krishna-Godavari Basin, East Coast of India. Microb. Ecol., 85 (1) (2023), pp. 61-75,

S. Seabrook, M.E. Torres, T. Baumberger, D. Butterfield, K. Roe, M. Cummings, A.R. Thurber. Ubiquitous but unique: Water depth and oceanographic attributes shape methane seep communities. Limnol. Oceanogr., 69 (5) (2024), pp. 1218-1232,

W. Serrano, R.M. Olaechea, L. Cerpa, J. Herrera, A. Indacochea. Bacterial diversity profiling around the Orca Seamount in the Bransfield Strait, Antarctica, based on 16S rRNA gene amplicon sequences. Microbiol. Resour. Announc., 10 (1) (2021), pp. 10-1128,

A.C. Semler, J.L. Fortney, R.W. Fulweiler, A.E. Dekas. Cold seeps on the passive Northern US Atlantic Margin host globally representative members of the seep microbiome with locally dominant strains of archaea. Appl. Environ. Microbiol., 88 (11) (2022), pp. e00468-e522,

A. Sen, S. Duperron, S. Hourdez, B. Piquet, N. Léger, A. Gebruk, A.C. Andersen. Cryptic frenulates are the dominant chemosymbiotrophic fauna at Arctic and high latitude Atlantic cold seeps. PLoS One, 13 (12) (2018), Article e0209273,

S. Shao, X. Luan, H. Dang, H. Zhou, Y. Zhao, H. Liu, M.G. Klotz. Deep-sea methane seep sediments in the Okhotsk Sea sustain diverse and abundant anammox bacteria. FEMS Microbiol. Ecol., 87 (2) (2014), pp. 503-516,

C. Shen, J. Xiong, H. Zhang, Y. Feng, X. Lin, X. Li, H. Chu. Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol. Biochem., 57 (2013), pp. 204-211,

Q.L. Sun, J. Zhang, M.X. Wang, L. Cao, Z.F. Du, Y.Y. Sun, L. Sun. High-throughput sequencing reveals a potentially novel Sulfurovum species dominating the microbial communities of the seawater–sediment interface of a deep-sea cold seep in South China Sea. Microorganisms, 8 (5) (2020), p. 687,

Q.L. Sun, K. Xu, L. Cao, Z. Du, M. Wang, L. Sun. Nitrogen and sulfur cycling driven by Campylobacterota in the sediment–water interface of deep-sea cold seep: a case in the South China Sea. Mol. Biol. Microbiol., 14 (4) (2023),

A.D. Syakti, M. Yani, N.V. Hidayati, A.S. Siregar, P. Doumenq, I.M. Made Sudiana. The bioremediation potential of hydrocarbonoclastic bacteria isolated from a mangrove contaminated by petroleum hydrocarbons on the cilacap coast, Indonesia. Bioremediat. J., 17 (1) (2013), pp. 11-20,

F.É. Sylvain, B. Cheaib, M. Llewellyn, T. Gabriel Correia, D. Barros Fagundes, A. Luis Val, N. Derome. pH drop impacts differentially skin and gut microbiota of the Amazonian fish tambaqui (Colossoma macropomum). Sci. Rep., 6 (1) (2016), p. 32032,

P.L. Tavormina, W. Ussler III, V.J. Orphan. Planktonic and sediment-associated aerobic methanotrophs in two seep systems along the North American margin. Appl. Environ. Microbiol., 74 (13) (2008), pp. 3985-3995,

B.M. Tripathi, M. Kim, A. Lai-Hoe, N.A. Shukor, R.A. Rahim, R. Go, J.M. Adams. pH dominates variation in tropical soil archaeal diversity and community structure. FEMS Microbiol. Ecol., 86 (2) (2013), pp. 303-311,

A. Unnikrishnan, P. Das, N.L. Thakur, P. Devi. Exploring depths: Metagenomic profiling of cold seep bacterial communities and the isolation of hydrocarbon-degrading microbes from the Cauvery-Mannar basin. Reg. Stud. Mar. Sci., 72, 103440 (2024),

F. Unfried, S. Becker, C.S. Robb, J.H. Hehemann, S. Markert, S.E. Heiden, T. Schweder. Adaptive mechanisms that provide competitive advantages to marine bacteroidetes during microalgal blooms. ISME J., 12 (12) (2018), pp. 2894-2906,

D.L. Valentine, D.C. Blanton, W.S. Reeburgh, M. Kastner. Water column methane oxidation adjacent to an area of active hydrate dissociation, Eel River Basin. Geochim. Cosmochim. Acta, 65 (16) (2001), pp. 2633-2640,

D.L. Valentine. Biogeochemistry and microbial ecology of methane oxidation in anoxic environments: a review. Antonie Van Leeuwenhoek, 81 (2002), pp. 271-282,

A. Vanreusel, A.C. Andersen, A. Boetius, D. Connelly, M.R. Cunha, C. Decker, et al.. Biodiversity of cold seep ecosystems along the European margins. Oceanography, 22 (1) (2009), pp. 110-127,

J. Venetz, O.M. Żygadłowska, W.K. Lenstra, N.A. van Helmond, G.H. Nuijten, A.J. Wallenius, A.J. Veraart. Versatile methanotrophs form an active methane biofilter in the oxycline of a seasonally stratified coastal basin. Environ. Microbiol., 25 (11) (2023), pp. 2277-2288,

A. Vigneron, P. Cruaud, P. Pignet, J.C. Caprais, M.A. Cambon-Bonavita, A. Godfroy, L. Toffin. Archaeal and anaerobic methane oxidizer communities in the Sonora Margin cold seeps, Guaymas Basin (Gulf of California). ISME J., 7 (8) (2013), pp. 1595-1608,

X. Wang, N. Li, D. Feng, Y. Hu, G. Bayon, Q. Liang, D. Chen. Using chemical compositions of sediments to constrain methane seepage dynamics: a case study from Haima cold seeps of the South China Sea. J. Asian Earth Sci., 168 (2018), pp. 137-144,

D. Wang, J. Li, L. Su, W. Shen, K. Feng, X. Peng, Y. Deng. Phylogenetic diversity of functional genes in deep-sea cold seeps: a novel perspective on metagenomics. Microbiome, 11 (1) (2023), p. 276,

F. Widdel, A.J.B. Zehnder. Biology of Anaerobic Microorganisms. Wiley Interscience, (1988), pp. pp. 469-581

L. Wöhlbrand, J.H. Jacob, M. Kube, M. Mussmann, R. Jarling, A. Beck, R. Rabus. Complete genome, catabolic sub‐proteomes and key‐metabolites of Desulfobacula toluolica Tol2, a marine, aromatic compound‐degrading, sulfate‐reducing bacterium. Environ. Microbiol., 15 (5) (2013), pp. 1334-1355,

J. Xiong, Y. Liu, X. Lin, H. Zhang, J. Zeng, J. Hou, H. Chu. Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environ. Microbiol., 14 (9) (2012), pp. 2457-2466,

S. Yang, Y. Lv, X. Liu, Y. Wang, Q. Fan, Z. Yang, Y. Zhang. Genomic and enzymatic evidence of acetogenesis by anaerobic methanotrophic archaea. Nat. Commun., 11 (1) (2020), pp. 1-11,

S. Yang, X. Wen, Y. Shi, S. Liebner, H. Jin, A. Perfumo. Hydrocarbon degraders establish at the costs of microbial richness, abundance and keystone taxa after crude oil contamination in permafrost environments. Sci. Rep., 6 (1) (2016), p. 37473,

K. Yanagawa, M. Kouduka, Y. Nakamura, A. Hachikubo, H. Tomaru, Y. Suzuki. Distinct microbial communities thriving in gas hydrate-associated sediments from the eastern Japan Sea. J. Asian Earth Sci., 90 (2014), pp. 243-249,

T.S. Yun, D. Fratta, J.C. Santamarina. Hydrate-bearing sediments from the Krishna− Godavari Basin: physical characterization, pressure core testing, and scaled production monitoring. Energ. Fuel., 24 (11) (2010), pp. 5972-5983,

X. Zhai, X. Shi, H. Cheng, P. Yao, B. Zhao, L. Chen, M. Yu. Horizontal and vertical heterogeneity of sediment microbial community in Site F cold seep, the South China Sea. Front. Marine Sci., 9 (2022), Article 957762,

Y. Zhang, X. Su, F. Chen, Y. Wang, L. Jiao, H. Dong, et al.. Microbial diversity in cold seep sediments from the northern South China Sea. Geosci. Front., 3 (3) (2012), pp. 301-316,

T. Zhang, X. Xiao, S. Chen, J. Zhao, Z. Chen, J. Feng, et al.. Active anaerobic archaeal methanotrophs in recently emerged cold seeps of northern South China Sea. Front. Microbiol., 11 (2020), Article 612135,

C. Zhang, Y.X. Fang, X. Yin, H. Lai, Z. Kuang, T. Zhang, et al.. The majority of microorganisms in gas hydrate-bearing subseafloor sediments ferment macromolecules. Microbiome, 11 (2023), p. 37,

Zheng, R., Cai, R., Liu, R., Liu, G., Sun, C., 2020. Bacteroidetes contribute to the carbon and nutrient cycling of deep sea through breaking down diverse glycans. BioRxiv 2020-11. https://doi.org/10.1101/2020.11.07.372516.

S. Zhong, J. Feng, J. Kong, Y. Huang, X. Chen, S. Zhang. Differences in bacterial co-occurrence networks and ecological niches at the surface sediments and bottom seawater in the Haima cold seep. Microorganisms, 11 (12) (2023), p. 3001,