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Hadal trench sediments as key ecological reservoir for prokaryotic evolution

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    1. Hadal zones serve as an ancient reservoir, harboring more ancient microbial lineages than non-hadal zones.

      Evolutionary distances correlate with depth differences, evidenced by vertical shift in genomic features.

      Hadal microbes likely exchange across trenches via deep-sea currents to maintain genetic connectivity.

      Divergence of typical ancient lineages predates the formation of contemporary oceanic trenches.

  • The evolutionary ecology of prokaryotes within oceanic trenches remains largely unexplored. Here, we analyzed 19,194 medium-quality prokaryotic metagenomic assembled genomes (MAGs) from sediments of the Diamantina, Kermadec, Yap and Mariana trenches. Hadal zones hosted relatively ancient phylogenetic lineages across most prokaryotic phyla compared to non-hadal zones. A linear correlation between depth differences and the pairwise patristic distances was observed inter/intra trenches, indicating a depth-dependent evolutionary boundary. This pattern was further reflected by a clear vertical shift of genomic features, including carbon/nitrogen atoms per amino-acid-residue side chain (C/N-ARSC), pseudogene density and non-synonymous to synonymous mutation ratio (pN/pS). Close phylogenomic relationships for MAGs among different trenches suggested a rapidly and continuously exchange, which was very likely facilitated by deep-sea currents. Molecular dating of hadal Nitrososphaeria and Alphaproteobacteria revealed a divergence of respective 2.2 and 1.8 billion years ago, earlier than the emergence of contemporary trenches, emphasized the hadal zone sediments as a crucial ecological reservoir for prokaryotic evolution.
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  • [1] Du M.R., Peng X.T., Zhang H.B., et al. (2021). Geology, environment, and life in the deepest part of the world’s oceans. The Innovation 2:100109. DOI:10.1016/j.xinn.2021.100109

    View in Article CrossRef Google Scholar

    [2] Bruun A.F. (1957). Deep sea and abyssal depths. Hedgpeth J. (ed). Treatise on marine ecology and paleoecology (Geological Society of America), pp: 641-673. DOI:10.1130/MEM67V1-p641

    View in Article Google Scholar

    [3] Liu R.L., Wang L., Wei Y.L., et al. (2018). The hadal biosphere: Recent insights and new directions. Deep Sea Res. II Top. Stud. Oceanogr. 155:11−18. DOI:10.1016/j.dsr2.2017.04.015

    View in Article CrossRef Google Scholar

    [4] Shephard L.E. and Bryant W.R. (1983). Geotechnical properties of lower trench inner-slope sediments. Tectonophysics 99:279−312. DOI:10.1016/0040-1951(83)90109-9

    View in Article CrossRef Google Scholar

    [5] Liu H. and Jing H.M. (2024). The vertical metabolic activity and community structure of prokaryotes along different water depths in the Kermadec and Diamantina trenches. Microorganisms 12:708. DOI:10.3390/microorganisms12040708

    View in Article CrossRef Google Scholar

    [6] Chen S., Xie Z., Yan K., et al. (2026). Integrated meta-omics reveals organic matter processing by bacteria in the dark ocean. Innov. Geosci. 4:100184. DOI:10.59717/j.xinn-geo.2026.100184

    View in Article CrossRef Google Scholar

    [7] Chen S.Y., Xu J., Cao J., et al. (2024). Depth-related microbial communities and functional genes in alpine permafrost. Innov. Life 2:100081. DOI:10.59717/j.xinn-life.2024.100081

    View in Article CrossRef Google Scholar

    [8] Lyons T.W., Tino C.J., Fournier G.P., et al. (2024). Co‐evolution of early Earth environments and microbial life. Nat. Rev. Microbiol. 22:572−586. DOI:10.1038/s41579-024-01044-y

    View in Article CrossRef Google Scholar

    [9] Angel M.V. (1982). Ocean trench conservation. Environmentalist 2:1−17. DOI:10.1007/BF02340472

    View in Article CrossRef Google Scholar

    [10] Xiao X., Zhao W.S., Song Z.W., et al. (2025). Microbial ecosystems and ecological driving forces in the deepest ocean sediments. Cell 188:1363−1377. DOI:10.1016/j.cell.2024.12.036

    View in Article CrossRef Google Scholar

    [11] Peoples L.M., Grammatopoulou E., Pombrol M., et al. (2019). Microbial community diversity within sediments from two geographically separated hadal trenches. Front. Microbiol. 10:347. DOI:10.3389/fmicb.2019.00347

    View in Article CrossRef Google Scholar

    [12] Gao Z.M., Huang J.M., Cui G.J., et al. (2019). In situ meta‐omic insights into the community compositions and ecological roles of hadal microbes in the Mariana Trench. Environ. Microbiol. 21:4092−4108. DOI:10.1111/1462-2920.14759

    View in Article CrossRef Google Scholar

    [13] Crawford A.J., Beccaluva L., Serri G., et al. (1986). Petrology, geochemistry and tectonic implications of volcanics dredged from the intersection of the Yap and Mariana trenches. Earth Planet. Sci. Lett. 80:265−280. DOI:10.1016/0012-821X(86)90110-X

    View in Article CrossRef Google Scholar

    [14] Stewart H.A. and Jamieson A.J. (2019). The five deeps: The location and depth of the deepest place in each of the world's oceans. Earth-Sci. Rev. 197:102896. DOI:10.1016/j.earscirev.2019.102896

    View in Article CrossRef Google Scholar

    [15] Pandey S., Bhagawati C., Dandapat S., et al. (2020). Surface chlorophyll anomalies associated with Indian Ocean Dipole and El Niño Southern Oscillation in North Indian Ocean: A case study of 2006-2007 event. Environ. Monit. Assess. 191:807. DOI:10.1007/s10661-019-7754-z

    View in Article CrossRef Google Scholar

    [16] Li D.H., Luo R.B., Liu C.M., et al. (2016). MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods 102:3-11. DOI:10.1016/j.ymeth.2016.02.020

    View in Article Google Scholar

    [17] Uritskiy G.V., DiRuggiero J. and Taylor J. (2018). MetaWRAP—A flexible pipeline for genome-resolved metagenomic data analysis. Microbiome 6:158. DOI:10.1186/s40168-018-0541-1

    View in Article CrossRef Google Scholar

    [18] Parks D.H., Imelfort M., Skennerton C.T., et al. (2015). CheckM: Assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25:1043−1055. DOI:10.1101/gr.186072.114

    View in Article CrossRef Google Scholar

    [19] Chaumeil P.A., Mussig A.J., Hugenholtz P., et al., (2020). GTDB-tk: A toolkit to classify genomes with the genome taxonomy database. Bioinformatics 36:1925-1927. DOI:10.1093/bioinformatics/btz848

    View in Article Google Scholar

    [20] Moody E.R.R., Álvarez-Carretero S., Mahendrarajah T.A., et al. (2024). The nature of the last universal common ancestor and its impact on the early Earth system. Nat. Ecol. Evol. 8:1654−1666. DOI:10.1038/s41559-024-02461-1

    View in Article CrossRef Google Scholar

    [21] Hyatt D., Chen G.L., Locascio P.F., et al. (2010). Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119. DOI:10.1186/1471-2105-11-119

    View in Article CrossRef Google Scholar

    [22] Altschul S.F., Madden T.L., Schäffer A.A., et al. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25:3389−3402. DOI:10.1093/nar/25.17.3389

    View in Article CrossRef Google Scholar

    [23] Katoh K. and Standley D.M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30:772−780. DOI:10.1093/molbev/mst010

    View in Article CrossRef Google Scholar

    [24] Capella-Gutiérrez S., Silla-Martínez J.M. and Gabaldón T. (2009). trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972−1973. DOI:10.1093/bioinformatics/btp348

    View in Article CrossRef Google Scholar

    [25] Minh B.Q., Schmidt H.A., Chernomor O., et al. (2020). IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37:1530−1534. DOI:10.1093/molbev/msaa015

    View in Article CrossRef Google Scholar

    [26] Syberg-Olsen M.J., Garber A.I., Keeling P.J., et al. (2022). Pseudofinder: Detection of pseudogenes in prokaryotic genomes. Mol. Biol. Evol. 39:msac153. DOI:10.1093/molbev/msac153

    View in Article CrossRef Google Scholar

    [27] Olm M.R., Crits C.A., Bouma G.K., et al. (2021). inStrain profiles population microdiversity from metagenomic data and sensitively detects shared microbial strains. Nat. Biotechnol. 39:727−736. DOI:10.1038/s41587-020-00797-0

    View in Article CrossRef Google Scholar

    [28] Li Y.D., Chen J.W., Lin Y.X. et al. (2024). Thaumarchaeota from deep-sea methane seeps provide novel insights into their evolutionary history and ecological implications. Microbiome 12:197. DOI:10.1186/s40168-024-01912-y

    View in Article CrossRef Google Scholar

    [29] Wang S.S. and Luo H.W. (2021). Dating Alphaproteobacteria evolution with eukaryotic fossils. Nat. Commun. 12:3324. DOI:10.1038/s41467-021-23645-4

    View in Article CrossRef Google Scholar

    [30] Martijn J., Vosseberg J., Guy L., et al. (2018). Deep mitochondrial origin outside the sampled alphaproteobacteria. Nature 557:101−105. DOI:10.1038/s41586-018-0059-5

    View in Article CrossRef Google Scholar

    [31] Yang Z. (2007). PAML 4: Phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24:1586−1591. DOI:10.1093/molbev/msm088

    View in Article CrossRef Google Scholar

    [32] Yang Y., Zhang C., Lenton T.M., et al. (2021). The evolution pathway of ammonia-oxidizing archaea shaped by major geological events. Mol. Biol. Evol. 38:3637−3648. DOI:10.1093/molbev/msab129

    View in Article CrossRef Google Scholar

    [33] Ren M.L., Feng X.Y., Huang Y.J., et al. (2019). Phylogenomics suggests oxygen availability as a driving force in Thaumarchaeota evolution. ISME J. 13:2150−2161. DOI:10.1038/s41396-019-0418-8

    View in Article CrossRef Google Scholar

    [34] Luo H.W. (2022). Estimating the divergence times of alphaproteobacteria based on mitochondrial endosymbiosis and eukaryotic fossils. Luo, H.W. (ed). Environmental Microbial Evolution. Methods in Molecular Biology. (Humana), pp: 95-116. DOI:10.1007/978-1-0716-2691-7_5

    View in Article Google Scholar

    [35] Takahashi S., Tomita J., Nishioka K., et al. (2014). Development of a prokaryotic universal primer for simultaneous analysis of bacteria and archaea using next-generation sequencing. PLoS One 9:e105592. DOI:10.1371/journal.pone.0105592

    View in Article CrossRef Google Scholar

    [36] Bolyen E., Rideout J.R., Dillon M.R., et al. (2019). Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37:852−857. DOI:10.1038/s41587-019-0209-9

    View in Article CrossRef Google Scholar

    [37] Jain C., Rodriguez-R L.M., Phillippy A.M., et al. (2018). High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat. Commun. 9:5114. DOI:10.1038/s41467-018-07641-9

    View in Article CrossRef Google Scholar

    [38] Ondov B.D., Treangen T.J., Melsted P., et al. (2016). Mash: Fast genome and metagenome distance estimation using MinHash. Genome Biol. 17:132. DOI:10.1186/s13059-016-0997-x

    View in Article CrossRef Google Scholar

    [39] Moshiri N. (2020). TreeSwift: A massively scalable Python tree package. SoftwareX. 11:100436. DOI:10.1016/j.softx.2020.100436

    View in Article CrossRef Google Scholar

    [40] Jiang H.C., Yu L., Xu H.Z., et al. (2020). Evaluation of global ocean models on simulating the deep western boundary current in the pacific. Atmosphere-Ocean 58:219−230. DOI:10.1080/07055900.2020.1789547

    View in Article CrossRef Google Scholar

    [41] Nunoura T., Takaki Y., Hirai M., et al. (2015). Hadal biosphere: Insight into the microbial ecosystem in the deepest ocean on Earth. Proc. Natl. Acad. Sci. USA 112:E1230−E1236. DOI:10.1073/pnas.1421816112

    View in Article CrossRef Google Scholar

    [42] Chu M., Liu J., Li H., et al. (2023). Earthquake-induced redistribution and reburial of microbes in the hadal trenches. Innov. Geosci. 1:100027. DOI:10.59717/j.xinn-geo.2023.100027

    View in Article CrossRef Google Scholar

    [43] Parks D.H., Chuvochina M., Rinke C., et al. (2022). GTDB: An ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy. Nucleic. Acids. Res. 50:D785−D794. DOI:10.1093/nar/gkab776

    View in Article CrossRef Google Scholar

    [44] Avni E. and Snir S. (2020). A new phylogenomic approach for quantifying horizontal gene transfer trends in prokaryotes. Sci. Rep. 10:12425. DOI:10.1038/s41598-020-62446-5

    View in Article CrossRef Google Scholar

    [45] Goodhead I. and Darby A.C. (2015). Taking the pseudo out of pseudogenes. Curr. Opin. Microbiol. 23:102−109. DOI:10.1016/j.mib.2014.11.012

    View in Article CrossRef Google Scholar

    [46] 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

    [47] Bragg J.G. and Hyder C.L. (2004). Nitrogen versus carbon use in prokaryotic genomes and proteomes. Proc. Biol. Sci. 271:S374−S377. DOI:10.1098/rsbl.2004.0193

    View in Article CrossRef Google Scholar

    [48] Palomo A., Dechesne A., Cordero O.X., et al. (2022). Evolutionary ecology of natural comammox Nitrospira populations. mSystems 7:e0113921. DOI:10.1128/msystems.01139-21

    View in Article CrossRef Google Scholar

    [49] Long H.A., Sung W. and Kucukyildirim S. (2018). Evolutionary determinants of genome-wide nucleotide composition. Nat. Ecol. Evol. 2:237−240. DOI:10.1038/s41559-017-0425-y

    View in Article CrossRef Google Scholar

    [50] 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:e0156922. DOI:10.1128/mbio.01569-22

    View in Article CrossRef Google Scholar

    [51] Wang K., Shen Y., Yang Y., et al. (2019). Morphology and genome of a snailfish from the Mariana Trench provide insights into deep-sea adaptation. Nat. Ecol. Evol. 3:823−833. DOI:10.1038/s41559-019-0864-8

    View in Article CrossRef Google Scholar

    [52] Brum J.R., Ignacio-Espinoza J.C., Roux S., et al. (2015). Patterns and ecological drivers of ocean viral communities. Science 348:1261498. DOI:10.1126/science.1261498

    View in Article CrossRef Google Scholar

    [53] Zhao F., Wang Y., Zheng S., et al. (2021). Patterns and drivers of microeukaryotic distribution along the North Equatorial Current from the Central Pacific Ocean to the South China Sea. Mar. Pollut. Bull. 165:112091. DOI:10.1016/j.marpolbul.2021.112091

    View in Article CrossRef Google Scholar

    [54] Villar E., Farrant G.K., Follows M. et al. (2015). Ocean plankton. Environmental characteristics of Agulhas rings affect interocean plankton transport. Science 348:1261447. DOI:10.1126/science.1261447

    View in Article CrossRef Google Scholar

    [55] Kawabe M. and Fujio S. (2010). Pacific Ocean circulation based on observation. J. Oceanogr. 66:389−403. DOI:10.1007/s10872-010-0034-8

    View in Article CrossRef Google Scholar

  • Cite this article:

    Li Y., Xiao Y., Liu H., et al. (2026). Hadal trench sediments as key ecological reservoir for prokaryotic evolution. The Innovation Life 4:100209. https://doi.org/10.59717/j.xinn-life.2026.100209
    Li Y., Xiao Y., Liu H., et al. (2026). Hadal trench sediments as key ecological reservoir for prokaryotic evolution. The Innovation Life 4:100209. https://doi.org/10.59717/j.xinn-life.2026.100209

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