A unique subseafloor microbiosphere in the Mariana Trench driven by episodic sedimentation

Abstract

Hadal trenches are characterized by enhanced and infrequent high-rate episodic sedimentation events that likely introduce not only labile organic carbon and key nutrients but also new microbes that significantly alter the subseafloor microbiosphere. Currently, the role of high-rate episodic sedimentation in controlling the composition of the hadal subseafloor microbiosphere is unknown. Here, analyses of carbon isotope composition in a ~ 750 cm long sediment core from the Challenger Deep revealed noncontinuous deposition, with anomalous ¹⁴C ages likely caused by seismically driven mass transport and the funneling effect of trench geomorphology. Microbial community composition and diverse enzyme activities in the upper ~ 27 cm differed from those at lower depths, probably due to sudden sediment deposition and differences in redox condition and organic matter availability. At lower depths, microbial population numbers, and composition remained relatively constant, except at some discrete depths with altered enzyme activity and microbial phyla abundance, possibly due to additional sudden sedimentation events of different magnitude. Evidence is provided of a unique role for high-rate episodic sedimentation events in controlling the subsurface microbiosphere in Earth’s deepest ocean floor and highlight the need to perform thorough analysis over a large depth range to characterize hadal benthic populations. Such depositional processes are likely crucial in shaping deep-water geochemical environments and thereby the deep subseafloor biosphere.

Keywords

Hadal subseafloor / Deep water sediment / Mariana Trench / Radiocarbon / Microbial community / Redox potential

References

[1] Bao R, Strasser M, McNichol AP, Haghipour N, McIntyre C, Wefer G, Eglinton TI. Tectonically-triggered sediment and carbon export to the Hadal zone. Nat Commun, 2018, 9: 121,

[2] Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 2014, 30: 2114-2120,

[3] Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, et al.. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol, 2019, 37: 852-857,

[4] Bushnell B. . BBMap: a fast, accurate, splice-aware aligner, 2014 Walnut Creek, CA LBNL Department of Energy Joint Genome Institute

[5] Cadillo-Quiroz H, Bräuer S, Yashiro E, Sun C, Yavitt J, Zinder S. Vertical profiles of methanogenesis and methanogens in two contrasting acidic peatlands in central New York State, USA. Environ Microbiol, 2006, 8: 1428-1440,

[6] Chen P, Zhou H, Huang Y, Xie Z, Zhang M, Wei Y, Li J, Ma Y, Luo M, Ding W, Cao J, Jiang T, Nan P, Fang J, Li X. Revealing the full biosphere structure and versatile metabolic functions in the deepest ocean sediment of the Challenger Deep. Genome Biol, 2021, 22: 207,

[7] Chen M, Li D-W, Zhang H, Wang Z, Zhao M. Distinct variations and mechanisms for terrestrial OC ¹⁴C-ages in the Eastern China marginal sea sediments since the last deglaciation. Quat Sci Rev, 2023, 315,

[8] Cheng H, Zhang Y, Guo Z, He X, Liu R, Zhu XY, Li J, Liu J, Zhang X-H. Microbial dimethylsulfoniopropionate cycling in deep sediment of the Mariana Trench. Appl Environ Microbiol, 2023, 89,

[9] Danovaro R, Della Croce N, Dell’Anno A, Pusceddu A. A depocenter of organic matter at 7800 m depth in the SE Pacific Ocean. Deep Sea Res Part I Oceanogr Res Pap, 2003, 50: 1411-1420,

[10] Davis J, Benner R. Seasonal trends in the abundance, composition and bioavailability of particulate and dissolved organic matter in the Chukchi/Beaufort Seas and western Canada Basin. Deep Sea Res Part II Top Stud Oceanogr, 2005, 52: 3396-3410,

[11] Deng L, Bölsterli D, Kristensen E, Meile C, Su C-C, Bernasconi SM, Seidenkrantz M-S, Glombitza C, Lagostina L, Han X, Jørgensen BB, Røy H, Lever MA. Macrofaunal control of microbial community structure in continental margin sediments. Proc Natl Acad Sci USA, 2020, 117: 15911-15922,

[12] D'Hondt S, Spivack AJ, Pockalny R, Ferdelman TG, Fischer JP, Kallmeyer J, Abrams LJ, Smith DC, Graham D, Hasiuk F, Schrum H, Stancin AM. Subseafloor sedimentary life in the South Pacific Gyre. Proc Natl Acad Sci USA, 2009, 106: 11651-11656,

[13] D’Hondt S, Pockalny R, Fulfer VM, Spivack AJ. Subseafloor life and its biogeochemical impacts. Nat Commun, 2019, 10: 3519,

[14] Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods, 2013, 10: 996-998,

[15] Estes ER, Pockalny R, D’Hondt S, Inagaki F, Morono Y, Murray RW, Nordlund D, Spivack AJ, Wankel SD, Xiao N, Hansel CM. Persistent organic matter in oxic subseafloor sediment. Nat Geosci, 2019, 12: 126-131,

[16] Fan S, Wang M, Ding W, Li YX, Zhang YZ, Zhang W. Scientific and technological progress in the microbial exploration of the hadal zone. Mar Life Sci Technol, 2022, 4: 127-137,

[17] Faust JC, Tessin A, Fisher BJ, Zindorf M, Papadaki S, Hendry KR, Doyle KA, März C. Millennial scale persistence of organic carbon bound to iron in Arctic marine sediments. Nat Commun, 2021, 12: 275,

[18] Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ, Millero FJ. Impact of anthropogenic CO₂ on the CaCO₃ system in the oceans. Science, 2004, 305: 362-366,

[19] Freitas L, Appolinario L, Calegario G, Campeão M, Tschoeke D, Garcia G, Venancio IM, Cosenza CAN, Leomil L, Bernardes M, Albuquerque AL, Thompson C, Thompson F. Glacial-interglacial transitions in microbiomes recorded in deep-sea sediments from the western equatorial Atlantic. Sci Total Environ, 2020, 746,

[20] Frossard A, Hammes F, Gessner MO. Flow cytometric assessment of bacterial abundance in soils, sediments and sludge. Front Microbiol, 2016, 7: 903,

[21] Ghai R, Mizuno CM, Picazo A, Camacho A, Rodriguez-Valera F. Metagenomics uncovers a new group of low GC and ultra-small marine Actinobacteria. Sci Rep, 2013, 3: 2471,

[22] Glud RN, Wenzhöfer F, Middelboe M, Oguri K, Turnewitsch R, Canfield DE, Kitazato H. High rates of microbial carbon turnover in sediments in the deepest oceanic trench on Earth. Nat Geosci, 2013, 6: 284-288,

[23] Hayes MA, Jesse A, Hawke B, Baldock J, Tabet B, Lockington D, Lovelock CE. Dynamics of sediment carbon stocks across intertidal wetland habitats of Moreton Bay, Australia. Glob Chang Biol, 2017, 23: 4222-4234,

[24] Heeszel DS, Wiens DA, Shore PJ, Shiobara H, Sugioka H. Earthquake evidence for along-arc extension in the Mariana Islands. Geochem Geophys Geosyst, 2008, 9: Q12X03,

[25] Hiraoka S, Hirai M, Matsui Y, Makabe A, Minegishi H, Tsuda M, Juliarni RE, Danovaro R, Corinaldesi C, Kitahashi T, Tasumi E, Nishizawa M, Takai K, Nomaki H, Nunoura T. Microbial community and geochemical analyses of trans-trench sediments for understanding the roles of hadal environments. ISME J, 2020, 14: 740-756,

[26] Jørgensen BB, Marshall IP. Slow microbial life in the seabed. Annu Rev Mar Sci, 2016, 8: 311-332,

[27] Kallmeyer J, Pockalny R, Adhikari RR, Smith DC, D’Hondt S. Global distribution of microbial abundance and biomass in subseafloor sediment. Proc Natl Acad Sci USA, 2012, 109: 16213-16216,

[28] Khalili B, Weihe C, Kimball S, Schmidt KT, Martiny JB. Optimization of a method to quantify soil bacterial abundance by flow cytometry. mSphere, 2019, 4: e00435-e519,

[29] Kioka A, Schwestermann T, Moernaut J, Ikehara K, Kanamatsu T, Eglinton TI, Strasser M. Event stratigraphy in a hadal oceanic trench: the Japan trench as sedimentary archive recording recurrent giant subduction zone earthquakes and their role in organic carbon export to the deep sea. Front Earth Sci, 2019, 7: 319,

[30] Könneke M, Bernhard AE, de La Torre JR, Walker CB, Waterbury JB, Stahl DA. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature, 2005, 437: 543-546,

[31] Kraft B, Jehmlich N, Larsen M, Bristow L, Könneke M, Thamdrup B, Canfield D. Oxygen and nitrogen production by an ammonia-oxidizing archaeon. Science, 2022, 375: 97-100,

[32] Li Y, Cao W, Wang Y, Ma Q. Microbial diversity in the sediments of the southern Mariana Trench. J Oceanol Limnol, 2019, 37: 1024-1029,

[33] Liang J, Liu J, Zhan Y, Zhou S, Xue C-X, Sun C, Lin Y, Luo C, Wang X, Zhang X-H. Succession of marine bacteria in response to Ulva prolifera-derived dissolved organic matter. Environ Int, 2021, 155,

[34] Liu J, Zheng Y, Lin H, Wang X, Li M, Liu Y, Yu M, Zhao M, Pedentchouk N, Lea-Smith DJ, Todd JD, Magill CR, Zhang WJ, Zhou S, Song D, Zhong H, Xin Y, Yu M, Tian J, Zhang X-H. Proliferation of hydrocarbon-degrading microbes at the bottom of the Mariana Trench. Microbiome, 2019, 7: 47,

[35] Liu R, Wei X, Song W, Wang L, Cao J, Wu J, Thomas T, Jin T, Wang Z, Wei W, Wei Y, Zhai H, Yao C, Shen Z, Du J, Fang J. Novel chloroflexi genomes from the deepest ocean reveal metabolic strategies for the adaptation to deep-sea habitats. Microbiome, 2022, 10: 75,

[36] López-Pérez M, Haro-Moreno JM, Iranzo J, Rodriguez-Valera F. Genomes of the “Candidatus Actinomarinales” order: highly streamlined marine epipelagic Actinobacteria. mSystems, 2020, 5: e01041-e1120,

[37] Luo M, Gieskes J, Chen L, Shi X, Chen D. Provenances, distribution, and accumulation of organic matter in the southern Mariana Trench rim and slope: implication for carbon cycle and burial in hadal trenches. Mar Geol, 2017, 386: 98-106,

[38] Luo M, Glud RN, Pan B, Wenzhöfer F, Xu Y, Lin G, Chen D. Benthic carbon mineralization in hadal trenches: insights from in situ determination of benthic oxygen consumption. Geophys Res Lett, 2018, 45: 2752-2760,

[39] Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 2011, 27: 2957-2963,

[40] Mahmoudi N, Hagen SM, Hazen TC, Steen AD. Patterns in extracellular enzyme activity and microbial diversity in deep-sea Mediterranean sediments. Deep Sea Res Part I Oceanogr Res Pap, 2020, 158,

[41] Martens-Habbena W, Berube PM, Urakawa H, de La Torre JR, Stahl DA. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature, 2009, 461: 976-979,

[43] Morono Y, Terada T, Masui N, Inagaki F. Discriminative detection and enumeration of microbial life in marine subsurface sediments. ISME J, 2009, 3: 503-511,

[44] Nunoura T, Nishizawa M, Hirai M, Shimamura S, Harnvoravongchai P, Koide O, Morono Y, Fukui T, Inagaki F, Miyazaki J, Takaki Y, Takai K. Microbial diversity in sediments from the bottom of the Challenger Deep, the Mariana Trench. Microbes Environ, 2018, 33: 186-194,

[45] Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. metaSPAdes: a new versatile metagenomic assembler. Genome Res, 2017, 27: 824-834,

[46] Orsi WD. Ecology and evolution of seafloor and subseafloor microbial communities. Nat Rev Microbiol, 2018, 16: 671-683,

[47] Orsi WD, Schink B, Buckel W, Martin WF. Physiological limits to life in anoxic subseafloor sediment. FEMS Microbiol Rev, 2020, 44: 219-231,

[48] Parkes RJ, Cragg B, Roussel E, Webster G, Weightman A, Sass H. A review of prokaryotic populations and processes in sub-seafloor sediments, including biosphere: geosphere interactions. Mar Geol, 2014, 352: 409-425,

[49] Peoples LM, Grammatopoulou E, Pombrol M, Xu X, Osuntokun O, Blanton J, Allen EE, Nunnally CC, Drazen JC, Mayor DJ, Bartlett DH. Microbial community diversity within sediments from two geographically separated hadal trenches. Front Microbiol, 2019, 10: 347,

[50] Qin W, Zheng Y, Zhao F, Wang Y, Urakawa H, Martens-Habbena W, Liu H, Huang X, Zhang X, Nakagawa T, Mende DR, Bollmann A, Wang B, Zhang Y, Amin SA, Nielsen JL, Mori K, Takahashi R, Virginia Armbrust E, Winkler MH, et al.. Alternative strategies of nutrient acquisition and energy conservation map to the biogeography of marine ammonia-oxidizing archaea. ISME J, 2020, 14: 2595-2609,

[51] Rastelli E, Corinaldesi C, Dell’Anno A, Tangherlini M, Lo Martire M, Nishizawa M, Nomaki H, Nunoura T, Danovaro R. Drivers of bacterial α-and β-diversity patterns and functioning in subsurface hadal sediments. Front Microbiol, 2019, 10: 2609,

[52] Schauberger C, Middelboe M, Larsen M, Peoples LM, Bartlett DH, Kirpekar F, Rowden AA, Wenzhöfer F, Thamdrup B, Glud RN. Spatial variability of prokaryotic and viral abundances in the Kermadec and Atacama Trench regions. Limnol Oceanogr, 2021, 66: 2095-2109,

[53] Schauberger C, Glud RN, Hausmann B, Trouche B, Maignien L, Poulain J, Wincker P, Arnaud-Haond S, Wenzhöfer F, Thamdrup B. Microbial community structure in hadal sediments: high similarity along trench axes and strong changes along redox gradients. ISME J, 2021, 15: 3455-3467,

[54] Schwestermann T, Eglinton TI, Haghipour N, McNichol AP, Ikehara K, Strasser M. Event-dominated transport, provenance, and burial of organic carbon in the Japan Trench. Earth Planet Sci Lett, 2021, 563,

[55] Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics, 2014, 30: 2068-2069,

[56] Shan S, Qi Y, Tian J, Wang X, Luo C, Zhou C, Zhang X-H, Xin Y, Wang Y. Carbon cycling in the deep Mariana Trench in the western north Pacific Ocean: insights from radiocarbon proxy data. Deep Sea Res Part I Oceanogr Res Pap, 2020, 164,

[57] Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ. Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA, 2006, 103: 12115-12120,

[58] Sun D-L, Jiang X, Wu QL, Zhou N-Y. Intragenomic heterogeneity of 16S rRNA genes causes overestimation of prokaryotic diversity. Appl Environ Microbiol, 2013, 79: 5962-5969,

[59] Thamdrup B, Schauberger C, Larsen M, Trouche B, Maignien L, Arnaud-Haond S, Wenzhöfer F, Glud RN. Anammox bacteria drive fixed nitrogen loss in hadal trench sediments. Proc Natl Acad Sci USA, 2021, 118,

[60] Turnewitsch R, Falahat S, Stehlikova J, Oguri K, Glud RN, Middelboe M, Kitazato H, Wenzhöfer F, Ando K, Fujio S, Yanagimoto D. Recent sediment dynamics in hadal trenches: evidence for the influence of higher-frequency (tidal, near-inertial) fluid dynamics. Deep Sea Res Part I Oceanogr Res Pap, 2014, 90: 125-138,

[61] Uritskiy GV, DiRuggiero J, Taylor J. MetaWRAP-a flexible pipeline for genome-resolved metagenomic data analysis. Microbiome, 2018, 6: 158,

[62] Vuillemin A, Kerrigan Z, D'Hondt S, Orsi WD. Exploring the abundance, metabolic potential and gene expression of subseafloor Chloroflexi in million-year-old oxic and anoxic abyssal clay. FEMS Microbiol Ecol, 2020, 96: fiaa223,

[63] Vuillemin A, Vargas S, Coskun OK, Pockalny R, Murray RW, Smith DC, D’Hondt S, Orsi WD. Atribacteria reproducing over millions of years in the Atlantic abyssal subseafloor. Mbio, 2020, 11: e01937-e2020,

[64] Walters W, Hyde ER, Berg-Lyons D, Ackermann G, Humphrey G, Parada A, Gilbert JA, Jansson JK, Caporaso JG, Fuhrman JA, Apprill A, Knight R. Improved bacterial 16S rRNA gene (V4 and V4–5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems, 2016, 1: e00009-15,

[65] Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol, 2007, 73: 5261-5267,

[66] Wenzhöfer F, Oguri K, Middelboe M, Turnewitsch R, Toyofuku T, Kitazato H, Glud RN. Benthic carbon mineralization in hadal trenches: assessment by in situ O2 microprofile measurements. Deep Sea Res Part I Oceanogr Res Pap, 2016, 116: 276-286,

[67] Wu J, Wang L, Du J, Liu Y, Hu L, Wei H, Fang J, Liu R. Biogeographic distribution, ecotype partitioning and controlling factors of Chloroflexi in the sediments of six hadal trenches of the Pacific Ocean. Sci Total Environ, 2023, 880,

[68] Xiao W, Xu Y, Haghipour N, Montluçon DB, Pan B, Jia Z, Ge H, Yao P, Eglinton TI. Efficient sequestration of terrigenous organic carbon in the New Britain Trench. Chem Geol, 2020, 533,

[69] Xu Y, Li X, Luo M, Xiao W, Fang J, Rashid H, Peng Y, Li W, Wenzhöfer F, Rowden AA, Glud RN. Distribution, source, and burial of sedimentary organic carbon in Kermadec and Atacama Trenches. J Geophys Res Biogeosci, 2021, 126,

[70] Xue C-X, Liu J, Lea-Smith DJ, Rowley G, Lin H, Zheng Y, Zhu X-Y, Liang J, Ahmad W, Todd JD, Zhang X-H. Insights into the vertical stratification of microbial ecological roles across the deepest seawater column on Earth. Microorganisms, 2020, 8: 1309,

[71] Xue C-X, Lin H, Zhu X-Y, Liu J, Zhang Y, Rowley G, Todd J, Li M, Zhang X-H. DiTing: a pipeline to infer and compare biogeochemical pathways from metagenomic and metatranscriptomic data. Front Microbiol, 2021, 12,

[72] Zhang Y, Yao P, Sun C, Li S, Shi X, Zhang XH, Liu J. Vertical diversity and association pattern of total, abundant and rare microbial communities in deep-sea sediments. Mol Ecol, 2021, 30: 2800-2816,

[73] Zhao R, Mogollón JM, Abby SS, Schleper C, Biddle JF, Roerdink DL, Thorseth IH, Jørgensen SL. Geochemical transition zone powering microbial growth in subsurface sediments. Proc Natl Acad Sci USA, 2020, 117: 32617-32626,

[74] Zhou J, Bruns MA, Tiedje JM. DNA recovery from soils of diverse composition. Appl Environ Microbiol, 1996, 62: 316-322,

[75] Zhou Y-L, Mara P, Cui G-J, Edgcomb VP, Wang Y. Microbiomes in the challenger deep slope and bottom-axis sediments. Nat Commun, 2022, 13: 1515,

[76] Zhu G, Yang H, Lin J, Zhou Z, Xu M, Sun J, Wan K. Along-strike variation in slab geometry at the southern Mariana subduction zone revealed by seismicity through ocean bottom seismic experiments. Geophys J Int, 2019, 218: 2122-2135,

[77] Zhu X-Y, Li Y, Xue C-X, Lidbury IDEA, Todd JD, Lea-Smith DJ, Tian J, Zhang X-H, Liu J. Deep-sea Bacteroidetes from the Mariana Trench specialize in hemicellulose and pectin degradation typically associated with terrestrial systems. Microbiome, 2023, 11: 175,