Integrated meta-omics reveals organic matter processing by bacteria in the dark ocean

Shi Chen; Zhang-Xian Xie; Ke-Qiang Yan; Jian-Wei Chen; Ling-Fen Kong; Dong-Xu Li; Peng-Fei Wu; Ling Peng; Lin Lin; Zihao Zhao; Guang-Yi Fan; Si-Qi Liu; Gerhard J. Herndl; Da-Zhi Wang

doi:10.59717/j.xinn-geo.2026.100184

The Innovation Geoscience > 2026 Vol. 4 > No. 1 > 100184

Next Article Previous Article

ARTICLE Open Access

Cite PDF

Integrated meta-omics reveals organic matter processing by bacteria in the dark ocean

1.
State Key Laboratory of Marine Environmental Science/College of the Environment and Ecology, Xiamen University, Xiamen 361005, China
2.
Department of Marine Technology, Rizhao Polytechnic, Rizhao 276826, China
3.
Key Laboratory of Rural Environmental Remediation and Waste Recycling/School of Resources and Environmental Sciences, Quanzhou Normal University, Quanzhou, 362000, China
4.
BGI-Research, Shenzhen 518083, China
5.
College of Life Sciences, University of Chinese Academy of Sciences, Beijing 100049, China
6.
Qingdao Key Laboratory of Marine Genomics, BGI-Research, Qingdao 266555, China
7.
Qingdao-Europe Advanced Institute for Life Sciences, BGI-Research, Qingdao 266555, China
8.
Department of Functional and Evolutionary Ecology, University of Vienna, Djerassiplatz 1, Vienna 1030, Austria
9.
NIOZ, Department of Marine Microbiology and Biogeochemistry, Royal Netherlands Institute for Sea Research, Utrecht University, Texel 1797 SZ , The Netherlands
10.
These authors contributed equally

Show all affliationsShow less

More Information

Corresponding authors: gerhard.herndl@univie.ac.at (G.H); dzwang@xmu.edu.cn (D.W.)
Received Date: February 21, 2025

Accepted Date: October 14, 2025

Published Online: October 17, 2025

The Innovation Geoscience 4(1), https://doi.org/10.59717/j.xinn-geo.2026.100184 | Cite this article

GRAPHICAL ABSTRACT

GRAPHICAL ABSTRACT

DownLoad: Full size image

PUBLIC SUMMARY

PUBLIC SUMMARY
1. Bacterial metabolisms for processing deep-sea organic matter are uncovered through integrated meta-omics.
  
  Dominant bacteria have different lifestyle preferences and metabolic niches in the deep sea.
  
  Alteromonadales, Oceanospirillales and Sphingomonadales are the major sharing bacteria.
  
  Rhodobacterales and Pelagibacterales are representative selfish and scavenging bacteria, respectively.
  
  Lifestyle and nutritive mode play key roles in bacteria-mediated organic matter processes in deep sea.

ABSTRACT

ABSTRACT

The dark ocean plays a critical role in organic matter cycling and global carbon sequestration; however, a detailed mechanistic understanding of the bacteria-mediated organic matter processes is still in its infancy. Here, we characterized the functional diversity, metabolic potential, and activities of particle-attached (PA, 1.6-200 µm) and free-living (FL, 0.2-1.6 µm) bacterial communities collected from a depth of 3,000 m at two sites with contrasting environments in the South China Sea using a combined metaproteomic and metagenomic approach. The taxonomic composition of the microbial communities varied between the two size fractions. Prominent bacterial groups exhibited distinct lifestyle preferences. Oceanospirillales preferred a PA lifestyle while Pelagibacterales favored an FL lifestyle. Moreover, the dominant bacterial groups occupied distinct metabolic niches in the remineralization of organic carbon. Alteromonadales, Oceanospirillales, and Sphingomonadales adopted a ‘sharing’ mode by expressing peptidases, non-proteolytic hydrolases, oxygenases, and dehydrogenases to cleave particulate organic matter into labile organic substrates presumably taken up by the enzyme-producing bacteria or by co-occurring bacteria. Rhodobacterales, however, exhibited a ‘selfish’ mode, and Pelagibacterales adopted a ‘scavenging’ mode, expressing only low and even no extracellular enzymes but abundant transporters to take up different ranges of available substrates. Role allocation among bacteria with varying life strategies and nutritive modes effectively drives organic matter processing in the dark ocean. Our results provide insights into the metabolic features, lifestyles, and nutritional strategies of deep-sea bacteria, thereby advancing our understanding of the biogeochemistry of organic matter driven by bacteria in the dark ocean.
- dark ocean /
- organic matter processing /
- bacteria /
- metaproteomics /
- metagenomics

FullText(HTML)

REFERENCES

[1]	Salazar G., Cornejo-Castillo F.M., Benitez-Barrios V., et al. (2016). Global diversity and biogeography of deep-sea pelagic prokaryotes. ISME J. 10:596−608. DOI:10.1038/ismej.2015.137 View in Article CrossRef Google Scholar
[2]	Arístegui J., Agustí S., Middelburg J.J., et al. (2005). Respiration in the mesopelagic and bathypelagic zones of the oceans. Del Giorgio P.A. and Williams P.J. le B. (eds). Respiration in Aquatic Ecosystems (Oxford University Press), pp.181-205. DOI: 10.1093/acprof:oso/9780198527084.003.0010 View in Article Google Scholar
[3]	Del Giorgio P.A. and Duarte C.M. (2002). Respiration in the open ocean. Nature 420:379−384. DOI:10.1038/nature01165 View in Article CrossRef Google Scholar
[4]	Herndl G.J. and Reinthaler T. (2013). Microbial control of the dark end of the biological pump. Nat. Geosci. 6:718−724. DOI:10.1038/NGEO1921 View in Article CrossRef Google Scholar
[5]	Herndl G.J., Bayer B., Baltar F., et al. (2023). Prokaryotic life in the deep ocean's water column. Ann. Rev. Mar. Sci. 15:461−483. DOI:10.1146/annurev-marine-032122-115655 View in Article CrossRef Google Scholar
[6]	Jiao N., Herndl G.J., Hansell D.A., et al. (2010). Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat. Rev. Microbiol. 8:593−599. DOI:10.1038/nrmicro2386 View in Article CrossRef Google Scholar
[7]	Arrieta J.M., Mayol E., Hansman R.L., et al. (2015). Dilution limits dissolved organic carbon utilization in the deep ocean. Science 348:331−333. DOI:10.1126/science.1258955 View in Article CrossRef Google Scholar
[8]	Druffel E.R. and Williams P.M. (1990). Identification of a deep marine source of particulate organic carbon using bomb 14C. Nature 347:172−174. DOI:10.1038/347172A0 View in Article CrossRef Google Scholar
[9]	Bergauer K., Fernandez-Guerra A., Garcia J.A.L., et al. (2018). Organic matter processing by microbial communities throughout the Atlantic water column as revealed by metaproteomics. Proc. Natl. Acad. Sci. USA 115:E400−E408. DOI:10.1073/pnas.1708779115 View in Article CrossRef Google Scholar
[10]	Ganesh S., Parris D.J., DeLong E.F., et al. (2014). Metagenomic analysis of size-fractionated picoplankton in a marine oxygen minimum zone. ISME J. 8:187−211. DOI:10.1038/ismej.2013.144 View in Article CrossRef Google Scholar
[11]	Hansell D.A., Carlson C.A. and Schlitzer R. (2012). Net removal of major marine dissolved organic carbon fractions in the subsurface ocean. Global Biogeochem. Cycles 26:GB1016. DOI:10.1029/2011gb004069 View in Article CrossRef Google Scholar
[12]	Salazar G., Cornejo-Castillo F.M., Borrull E., et al. (2015). Particle-association lifestyle is a phylogenetically conserved trait in bathypelagic prokaryotes. Mol. Ecol. 24:5692−5706. DOI:10.1111/mec.13419 View in Article CrossRef Google Scholar
[13]	Zhao Z., Baltar F. and Herndl G.J. (2020). Linking extracellular enzymes to phylogeny indicates a predominantly particle-associated lifestyle of deep-sea prokaryotes. Sci. Adv. 6:eaaz4354. DOI:10.1126/sciadv.aaz4354 View in Article CrossRef Google Scholar
[14]	Kong L.F., Yan K.Q., Xie Z.X., et al. (2021). Metaproteomics reveals similar vertical distribution of microbial transport proteins in particulate organic matter throughout the water column in the northwest Pacific Ocean. Front. Microbiol. 12:629802. DOI:10.3389/fmicb.2021.629802 View in Article CrossRef Google Scholar
[15]	Liu Y., Liu X., Long Y., et al. (2023). Variations in dissolved organic matter chemistry on a vertical scale in the eastern Indian Ocean. Water Res. 232:119674. DOI:10.1016/j.watres.2023.119674 View in Article CrossRef Google Scholar
[16]	Sala M.M., Ruiz-Gonzalez C., Borrull E., et al. (2020). Prokaryotic capability to use organic substrates across the global tropical and subtropical ocean. Front. Microbiol. 11:918. DOI:10.3389/fmicb.2020.00918 View in Article CrossRef Google Scholar
[17]	Reintjes G., Arnosti C., Fuchs B., et al. (2019). Selfish, sharing and scavenging bacteria in the Atlantic Ocean: a biogeographical study of bacterial substrate utilisation. ISME J. 13:1119−1132. DOI:10.1038/s41396-018-0326-3 View in Article CrossRef Google Scholar
[18]	Giljan G., Brown S., Lloyd C.C., et al. (2023). Selfish bacteria are active throughout the water column of the ocean. ISME Commun. 3:11. DOI:10.1038/s43705-023-00219-7 View in Article CrossRef Google Scholar
[19]	Kong L.F., He Y.B., Xie Z.X., et al. (2021). Illuminating key microbial players and metabolic processes involved in the remineralization of particulate organic carbon in the ocean’s twilight zone by metaproteomics. Appl. Environ. Microbiol. 87:e00986−00921. DOI:10.1128/AEM.00986-21 View in Article CrossRef Google Scholar
[20]	Wong G.T.F., Ku T.-L., Mulholland M., et al. (2007). The SouthEast Asian Time-series Study (SEATS) and the biogeochemistry of the South China Sea—An overview. Deep Sea Res. PT. II 54:1434−1447. DOI:10.1016/j.dsr2.2007.05.012 View in Article CrossRef Google Scholar
[21]	Dai M., Li X., Zhang Y., et al. (2024). Dissolved organic carbon in the South China Sea. Hansell D.A. and Carlson C.A. (eds). Biogeochemistry of marine dissolved organic matter (Elsevier), pp. 739-767. DOI: 10.1016/b978-0-443-13858-4.00002-2 View in Article Google Scholar
[22]	Li J., Gu L., Bai S., et al. (2021). Characterization of particle-associated and free-living bacterial and archaeal communities along the water columns of the South China Sea. Biogeosciences 18:113−133. DOI:10.5194/bg-18-113-2021 View in Article CrossRef Google Scholar
[23]	Zhang Y., Zhao Z., Dai M., et al. (2014). Drivers shaping the diversity and biogeography of total and active bacterial communities in the South China Sea. Mol. Ecol. 23:2260−2274. DOI:10.1111/mec.12739 View in Article CrossRef Google Scholar
[24]	Ma W., Chai F., Xiu P., et al. (2014). Simulation of export production and biological pump structure in the South China Sea. Geo-Marine Letters 34:541−554. DOI:10.1007/s00367-014-0384-0 View in Article CrossRef Google Scholar
[25]	Ma Y., Zhou K., Chen W., et al. (2023). Partitioning of carbon export in the euphotic zone of the oligotrophic South China Sea. Biogeosciences 20:2013−2030. DOI:10.5194/bg-20-2013-2023 View in Article CrossRef Google Scholar
[26]	Chen S., He Y.B., Xie Z.X., et al. (2021). Metaproteomics reveals nutrient availability shaping distinct microbial community and metabolic niche in the nutrient-depleted and replete layers of an oligotrophic euphotic zone. Sci. Total Environ. 774:145123. DOI:10.1016/j.scitotenv.2021.145123 View in Article CrossRef Google Scholar
[27]	Gordon L.I., Jennings Jr J.C., Ross A.A., et al. (1993). A suggested protocol for continuous flow automated analysis of seawater nutrients (phosphate, nitrate, nitrite and silicic acid) in the WOCE Hydrographic Program and the Joint Global Ocean Fluxes Study. WOCE hydrographic program office, methods manual WHPO1-52 View in Article Google Scholar
[28]	Hingamp P., Grimsley N., Acinas S.G., et al. (2013). Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes. ISME J. 7:1678−1695. DOI:10.1038/ismej.2013.59 View in Article CrossRef Google Scholar
[29]	Dong H.P., Wang D.Z., Dai M., et al. (2010). Characterization of particulate organic matter in the water column of the South China Sea using a shotgun proteomic approach. Limnol. Oceanogr. 55:1565−1578. DOI:10.4319/lo.2010.55.4.1565 View in Article CrossRef Google Scholar
[30]	Chen S., Xie Z.X., Yan K.Q., et al. (2024). Functional vertical connectivity of microbial communities in the ocean. Sci. Adv. 10:eadj8184. DOI:10.1126/sciadv.adj8184 View in Article CrossRef Google Scholar
[31]	Huson D.H., Mitra S., Ruscheweyh H.-J., et al. (2011). Integrative analysis of environmental sequences using MEGAN4. Genome Res. 21:1552−1560. DOI:10.1101/gr.120618.111 View in Article CrossRef Google Scholar
[32]	Kanehisa M., Furumichi M., Tanabe M., et al. (2017). KEGG: New perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 45:D353−D361. DOI:10.1093/nar/gkw1092 View in Article CrossRef Google Scholar
[33]	Zhang H., Wang D.Z., Xie Z.X., et al. (2015). Comparative proteomics reveals highly and differentially expressed proteins in field-collected and laboratory-cultured blooming cells of the diatom Skeletonema costatum. Environ. Microbiol. 17:3976−3991. DOI:10.1111/1462-2920.12914 View in Article CrossRef Google Scholar
[34]	Zhang X., Ning Z., Mayne J., et al. (2016). MetaPro-IQ: A universal metaproteomic approach to studying human and mouse gut microbiota. Microbiome 4:31. DOI:10.1186/s40168-016-0176-z View in Article CrossRef Google Scholar
[35]	Cox J. and Mann M. (2008). MaxQuant enables high peptide identification rates, individualized ppb-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26:1367−1372. DOI:10.1038/nbt.1511 View in Article CrossRef Google Scholar
[36]	Nakai K. and Horton P. (1999). PSORT: A program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem. Sci. 24:34−36. DOI:10.1016/S0968-0004(98)01336-X View in Article CrossRef Google Scholar
[37]	Suter E.A., Pachiadaki M., Taylor G.T., et al. (2018). Free‐living chemoautotrophic and particle‐attached heterotrophic prokaryotes dominate microbial assemblages along a pelagic redox gradient. Environ. Microbiol. 20:693−712. DOI:10.1111/1462-2920.13997 View in Article CrossRef Google Scholar
[38]	Acinas S.G., Sanchez P., Salazar G., et al. (2021). Deep ocean metagenomes provide insight into the metabolic architecture of bathypelagic microbial communities. Commun. Biol. 4:604. DOI:10.1038/s42003-021-02112-2 View in Article CrossRef Google Scholar
[39]	Dong C., Lai Q., Liu X., et al. (2021). Alcanivorax profundimaris sp. nov., a novel marine hydrocarbonoclastic bacterium isolated from seawater and deep-sea sediment. Curr. Microbiol. 78:1053−1060. DOI:10.1007/s00284-020-02322-7 View in Article CrossRef Google Scholar
[40]	Dong C., Wei L., Wang J., et al. (2022). Genome-based taxonomic rearrangement of Oceanobacter-related bacteria including the description of Thalassolituus hydrocarbonoclasticus sp. nov. and Thalassolituus pacificus sp. nov. and emended description of the genusThalassolituus.Front. Microbiol. 13:1051202. DOI:10.3389/fmicb.2022.1051202 View in Article CrossRef Google Scholar
[41]	Giovannoni S.J., Tripp H.J., Givan S., et al. (2005). Genome streamlining in a cosmopolitan oceanic bacterium. Science 309:1242−1245. DOI:10.1126/science.1114057 View in Article CrossRef Google Scholar
[42]	Zhao X., Schwartz C.L., Pierson J., et al. (2017). Three-dimensional structure of the ultraoligotrophic marine bacterium "Candidatus Pelagibacter ubique". Appl. Environ. Microbiol. 83:e02807−02816. DOI:10.1128/AEM.02807-16 View in Article CrossRef Candidatus Pelagibacter ubique"" target="_blank">Google Scholar
[43]	Padilla C.C., Ganesh S., Gantt S., et al. (2015). Standard filtration practices may significantly distort planktonic microbial diversity estimates. Front. Microbiol. 6:547. DOI:10.3389/fmicb.2015.00547 View in Article CrossRef Google Scholar
[44]	Shen Y., Benner R., Broek T.A., et al. (2025). Special delivery of proteinaceous matter to deep-sea microbes. Sci. Adv. 11:eadr0736. DOI:10.1126/sciadv.adr0736 View in Article CrossRef Google Scholar
[45]	Dang Y.R., Cha Q.Q., Liu S.S., et al. (2024). Phytoplankton-derived polysaccharides and microbial peptidoglycans are key nutrients for deep-sea microbes in the Mariana Trench. Microbiome 12:77. DOI:10.1186/s40168-024-01789-x View in Article CrossRef Google Scholar
[46]	Leu A.O., Eppley J.M., Burger A., et al. (2022). Diverse genomic traits differentiate sinking-particle-associated versus free-living microbes throughout the oligotrophic open ocean water column. mBio 13:e01569−01522. DOI:10.1128/mbio.01569-22 View in Article CrossRef Google Scholar
[47]	Smith D.C., Simon M., Alldredge A.L., et al. (1992). Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature 359:139−142. DOI:10.1038/359139a0 View in Article CrossRef Google Scholar
[48]	Hou L., Zhao Z., Steger-Mahnert B., et al. (2025). Microbial metabolism in laboratory reared marine snow as revealed by a multi-omics approach. Microbiome 13:114. DOI:10.1186/s40168-025-02097-8 View in Article CrossRef Google Scholar
[49]	Liu Q., Fang J., Li J., et al. (2018). Depth-resolved variations of cultivable bacteria and their extracellular enzymes in the water column of the New Britain Trench. Front. Microbiol. 9:135. DOI:10.3389/fmicb.2018.00135 View in Article CrossRef Google Scholar
[50]	Phale P.S., Basu A., Majhi P.D., et al. (2007). Metabolic diversity in bacterial degradation of aromatic compounds. Omics 11:252−279. DOI:10.1089/omi.2007.0004 View in Article CrossRef Google Scholar
[51]	Landry Z., Swan B.K., Herndl G.J., et al. (2017). SAR202 genomes from the dark ocean predict pathways for the oxidation of recalcitrant dissolved organic matter. mBio 8:e00413−00417. DOI:10.1128/mBio.00413-17 View in Article CrossRef Google Scholar
[52]	Cafaro V., Izzo V., Notomista E., et al. (2013). Marine hydrocarbonoclastic bacteria. Trincone A. (ed). Marine enzymes for biocatalysis (Woodhead Publishing), pp.373-402. DOI: 10.1533/9781908818355.3.373. View in Article Google Scholar
[53]	Moore E.R., Weaver A.J., Davis E.W., et al. (2022). Metabolism of key atmospheric volatile organic compounds by the marine heterotrophic bacterium Pelagibacter HTCC1062 (SAR11). Environ. Microbiol. 24:212−222. DOI:10.1111/1462-2920.15837 View in Article CrossRef Google Scholar
[54]	Ehrt S., Schirmer F. and Hillen W. (1995). Genetic organization, nucleotide sequence and regulation of expression of genes encoding phenol hydroxylase and catechol 1, 2‐dioxygenase in Acinetobacter calcoaceticus NCIB8250. Mol. Microbiol. 18:13−20. DOI:10.1111/j.1365-2958.1995.mmi_18010013.x View in Article CrossRef Google Scholar
[55]	Kita A., Kita S.-i., Fujisawa I., et al. (1999). An archetypical extradiol-cleaving catecholic dioxygenase: the crystal structure of catechol 2, 3-dioxygenase (metapyrocatechase) from Pseudomonas putida mt-2. Structure 7:25−34. DOI:10.1016/S0969-2126(99)80006-9 View in Article CrossRef Google Scholar
[56]	Rosas-Diaz J., Escobar-Zepeda A., Adaya L., et al. (2021). Paenarthrobacter sp. GOM3 is a novel marine species with monoaromatic degradation relevance. Front. Microbiol. 12:713702. DOI: 10.3389/fmicb.2021.713702 View in Article Google Scholar
[57]	Campbell J.W., Morgan‐Kiss R.M. and Cronan Jr J.E. (2003). A new Escherichia coli metabolic competency: Growth on fatty acids by a novel anaerobic β‐oxidation pathway. Mol. Microbiol. 47:793−805. DOI:10.1046/j.1365-2958.2003.03341.x View in Article CrossRef Google Scholar
[58]	Ivars-Martinez E., Martin-Cuadrado A.-B., D'auria G., et al. (2008). Comparative genomics of two ecotypes of the marine planktonic copiotroph Alteromonas macleodii suggests alternative lifestyles associated with different kinds of particulate organic matter. ISME J. 2:1194−1212. DOI:10.1038/ismej.2008.74 View in Article CrossRef Google Scholar
[59]	Guibert L.M., Loviso C.L., Marcos M.S., et al. (2012). Alkane biodegradation genes from chronically polluted subantarctic coastal sediments and their shifts in response to oil exposure. Microb. Ecol. 64:605−616. DOI:10.1007/s00248-012-0051-9 View in Article CrossRef Google Scholar
[60]	Teramoto M., Suzuki M., Okazaki F., et al. (2009). Oceanobacter-related bacteria are important for the degradation of petroleum aliphatic hydrocarbons in the tropical marine environment. Microbiology 155:3362−3370. DOI:10.1099/mic.0.030411-0 View in Article CrossRef Google Scholar

Cited by

ABOUT THIS ARTICLE

Cite this article:

Chen S., Xie Z., Yan K., et al. (2026). Integrated meta-omics reveals organic matter processing by bacteria in the dark ocean. The Innovation Geoscience 4:100184. https://doi.org/10.59717/j.xinn-geo.2026.100184

Chen S., Xie Z., Yan K., et al. (2026). Integrated meta-omics reveals organic matter processing by bacteria in the dark ocean. The Innovation Geoscience 4:100184. https://doi.org/10.59717/j.xinn-geo.2026.100184

Welcome!

To request copyright permission to republish or share portions of our works, please visit Copyright Clearance Center's (CCC) Marketplace website at marketplace.copyright.com.

Standard PDF

Extended PDF

Figures(7)

Article Metrics

Article views(1713) PDF downloads(467)

Integrated meta-omics reveals organic matter processing by bacteria in the dark ocean

GRAPHICAL ABSTRACT

PUBLIC SUMMARY

ABSTRACT

REFERENCES

ABOUT THIS ARTICLE

Cite this article:

Welcome!

Share

Article Metrics

Relative Articles

Cited by

Catalog

{{newsColumn.name}}

Journal links

{{newsColumn.name}}

Stay connected

Integrated meta-omics reveals organic matter processing by bacteria in the dark ocean

GRAPHICAL ABSTRACT

PUBLIC SUMMARY

ABSTRACT

REFERENCES

ABOUT THIS ARTICLE

Cite this article:

Welcome!

Share

Article Metrics

Relative Articles

Cited by

Catalog

Export File

Citation

Format

Content

{{newsColumn.name}}

Journal links

{{newsColumn.name}}

Stay connected