Biogeochemical and Microbial Variation across 5500 km of Antarctic Surface Sediment Implicates Organic Matter as a Driver of Benthic Community Structure

Western Antarctica, one of the fastest warming locations on Earth, is a unique environment that is underexplored with regards to biodiversity. Although pelagic microbial communities in the Southern Ocean and coastal Antarctic waters have been well-studied, there are fewer investigations of benthic communities and most have a focused geographic range. We sampled surface sediment from 24 sites across a 5500 km region of Western Antarctica (covering the Ross Sea to the Weddell Sea) to examine relationships between microbial communities and sediment geochemistry. Sequencing of the 16S and 18S rRNA genes showed microbial communities in sediments from the Antarctic Peninsula (AP) and Western Antarctica (WA), including the Ross, Amundsen, and Bellingshausen Seas, could be distinguished by correlations with organic matter concentrations and stable isotope fractionation (total organic carbon; TOC, total nitrogen; TN, and δ13C). Overall, samples from the AP were higher in nutrient content (TOC, TN, and NH4+) and communities in these samples had higher relative abundances of operational taxonomic units (OTUs) classified as the diatom, Chaetoceros, a marine cercozoan, and four OTUs classified as Flammeovirgaceae or Flavobacteria. As these OTUs were strongly correlated with TOC, the data suggests the diatoms could be a source of organic matter and the Bacteroidetes and cercozoan are grazers that consume the organic matter. Additionally, samples from WA have lower nutrients and were dominated by Thaumarchaeota, which could be related to their known ability to thrive as lithotrophs. This study documents the largest analysis of benthic microbial communities to date in the Southern Ocean, representing almost half the continental shoreline of Antarctica, and documents trophic interactions and coupling of pelagic and benthic communities. Our results indicate potential modifications in carbon sequestration processes related to change in community composition, identifying a prospective mechanism that links climate change to carbon availability.

[1]  A. L. Rice,et al.  Seasonal sedimentation of phytoplankton to the deep-sea benthos , 1983, Nature.

[2]  A. Mehlich Mehlich 3 soil test extractant: A modification of Mehlich 2 extractant , 1984 .

[3]  G. Fischer,et al.  Seasonal particle flux in the Bransfield Strait, Antartica , 1988 .

[4]  H. A. Thomsen,et al.  Fine structure and biology of Cryothecomonas gen. nov. (Protista incertae sedis) from the ice biota , 1991 .

[5]  P. Meyers Preservation of elemental and isotopic source identification of sedimentary organic matter , 1994 .

[6]  E. Delong,et al.  High abundance of Archaea in Antarctic marine picoplankton , 1994, Nature.

[7]  W. Smith,et al.  Hyperproductivity of the Ross Sea (Antarctica) polynya during austral spring , 1997 .

[8]  E. Delong,et al.  Seasonal and Spatial Variability of Bacterial and Archaeal Assemblages in the Coastal Waters near Anvers Island, Antarctica , 1998, Applied and Environmental Microbiology.

[9]  Kevin R. Arrigo,et al.  Primary production in Southern Ocean waters , 1998 .

[10]  J. T. Staley,et al.  Isolation of Marine Polycyclic Aromatic Hydrocarbon (PAH)-Degrading Cycloclasticus Strains from the Gulf of Mexico and Comparison of Their PAH Degradation Ability with That of Puget Sound Cycloclasticus Strains , 1998, Applied and Environmental Microbiology.

[11]  R. Collier,et al.  Particle fluxes to the interior of the Southern Ocean in the Western Pacific sector along 170°W , 2000 .

[12]  Ø. Hammer,et al.  PAST: PALEONTOLOGICAL STATISTICAL SOFTWARE PACKAGE FOR EDUCATION AND DATA ANALYSIS , 2001 .

[13]  S. Harayama,et al.  Bacteria Belonging to the Genus Cycloclasticus Play a Primary Role in the Degradation of Aromatic Hydrocarbons Released in a Marine Environment , 2002, Applied and Environmental Microbiology.

[14]  D. Kirchman The ecology of Cytophaga-Flavobacteria in aquatic environments. , 2002, FEMS microbiology ecology.

[15]  M. Vernet,et al.  Glacial meltwater dynamics in coastal waters west of the Antarctic peninsula , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[16]  G. Dieckmann,et al.  Particulate organic matter in Antarctic summer sea ice: concentration and stable isotopic composition , 2002 .

[17]  S. Giovannoni,et al.  High-Throughput Methods for Culturing Microorganisms in Very-Low-Nutrient Media Yield Diverse New Marine Isolates , 2002, Applied and Environmental Microbiology.

[18]  James E. Cloern,et al.  Stable carbon and nitrogen isotope composition of aquatic and terrestrial plants of the San Francisco Bay estuarine system , 2002 .

[19]  Ian Snape,et al.  Microbial community variation in pristine and polluted nearshore Antarctic sediments. , 2003, FEMS microbiology ecology.

[20]  J. Bowman,et al.  Prokaryotic Metabolic Activity and Community Structure in Antarctic Continental Shelf Sediments , 2003, Applied and Environmental Microbiology.

[21]  J. Bowman,et al.  Biodiversity, Community Structural Shifts, and Biogeography of Prokaryotes within Antarctic Continental Shelf Sediment , 2003, Applied and Environmental Microbiology.

[22]  T. Z. DeSantis,et al.  Comprehensive aligned sequence construction for automated design of effective probes (CASCADE-P) using 16S rDNA , 2003, Bioinform..

[23]  J. Pawlowski,et al.  Unexpected Foraminiferal Diversity Revealed by Small-subunit rDNA Analysis of Antarctic Sediment , 2004, The Journal of eukaryotic microbiology.

[24]  K. Arrigo Marine microorganisms and global nutrient cycles , 2005, Nature.

[25]  C. Heip,et al.  Biodiversity links above and below the marine sediment–water interface that may influence community stability , 2004, Biodiversity & Conservation.

[26]  Radhey S. Gupta,et al.  The Phylogeny and Signature Sequences Characteristics of Fibrobacteres, Chlorobi, and Bacteroidetes , 2004, Critical reviews in microbiology.

[27]  M. Könneke,et al.  Isolation of an autotrophic ammonia-oxidizing marine archaeon , 2005, Nature.

[28]  J. Bowman,et al.  Ecological and biogeographic relationships of class Flavobacteria in the Southern Ocean. , 2005, FEMS microbiology ecology.

[29]  D. DeMaster,et al.  A synthesis of bentho-pelagic coupling on the Antarctic shelf: Food banks, ecosystem inertia and global climate change , 2006 .

[30]  R. Bindschadler Antarctic Ice Sheet: Setting the Stage the Environment and Evolution of the West References Rapid Response Email Alerting Service the Environment and Evolution of the West Antarctic Ice Sheet: Setting the Stage , 2022 .

[31]  Eoin L. Brodie,et al.  Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB , 2006, Applied and Environmental Microbiology.

[32]  Marc Strous,et al.  Archaeal nitrification in the ocean , 2006, Proceedings of the National Academy of Sciences.

[33]  M. I. Wallace,et al.  Spatial and temporal variation in shallow seawater temperatures around Antarctica , 2006 .

[34]  S. Stammerjohn,et al.  Water-column processes in the West Antarctic Peninsula and the Ross Sea: Interannual variations and foodweb structure , 2006 .

[35]  R. Amann,et al.  Whole genome analysis of the marine Bacteroidetes'Gramella forsetii' reveals adaptations to degradation of polymeric organic matter. , 2006, Environmental microbiology.

[36]  T. Urich,et al.  Archaea predominate among ammonia-oxidizing prokaryotes in soils , 2006, Nature.

[37]  F. Azam,et al.  Microbial structuring of marine ecosystems , 2007, Nature Reviews Microbiology.

[38]  P. Legendre,et al.  vegan : Community Ecology Package. R package version 1.8-5 , 2007 .

[39]  Kamran Shalchian-Tabrizi,et al.  Phylogenomics Reshuffles the Eukaryotic Supergroups , 2007, PloS one.

[40]  A. Boetius,et al.  Feast and famine — microbial life in the deep-sea bed , 2007, Nature Reviews Microbiology.

[41]  B. Danis,et al.  The archaebacterial communities in Antarctic bathypelagic sediments , 2007 .

[42]  Kenneth L. Smith,et al.  Free-Drifting Icebergs: Hot Spots of Chemical and Biological Enrichment in the Weddell Sea , 2007, Science.

[43]  Francesca Malfatti,et al.  Microbial structuring of marine ecosystems , 2007, Nature Reviews Microbiology.

[44]  R. Jeffreys,et al.  Trophic structure on the West Antarctic Peninsula shelf: Detritivory and benthic inertia revealed by δ13C and δ15N analysis , 2008 .

[45]  Tianfeng Tan,et al.  A pyrene-degrading consortium from deep-sea sediment of the West Pacific and its key member Cycloclasticus sp. P1. , 2008, Environmental microbiology.

[46]  E. Delong,et al.  The Microbial Engines That Drive Earth's Biogeochemical Cycles , 2008, Science.

[47]  D. DeMaster,et al.  The FOODBANCS project: Introduction and sinking fluxes of organic carbon, chlorophyll-a and phytodetritus on the western Antarctic Peninsula continental shelf , 2008 .

[48]  Susan M. Huse,et al.  A Method for Studying Protistan Diversity Using Massively Parallel Sequencing of V9 Hypervariable Regions of Small-Subunit Ribosomal RNA Genes , 2009, PloS one.

[49]  R. Amann,et al.  Biogeography and phylogeny of the NOR5/OM60 clade of Gammaproteobacteria. , 2009, Systematic and applied microbiology.

[50]  R. Fani,et al.  Biochemical and microbial features of shallow marine sediments along the Terra Nova Bay (Ross Sea, Antarctica) , 2010 .

[51]  C. Bienhold,et al.  Bacterial diversity and biogeography in deep-sea surface sediments of the South Atlantic Ocean , 2010, The ISME Journal.

[52]  E. Sintes,et al.  Relevance of a crenarchaeotal subcluster related to Candidatus Nitrosopumilus maritimus to ammonia oxidation in the suboxic zone of the central Baltic Sea , 2010, The ISME Journal.

[53]  J. Aislabie,et al.  Crenarchaeota affiliated with group 1.1b are prevalent in coastal mineral soils of the Ross Sea region of Antarctica. , 2010, Environmental microbiology.

[54]  Patricia P. Chan,et al.  Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea , 2010, Proceedings of the National Academy of Sciences.

[55]  B. Scheuchl,et al.  Ice Flow of the Antarctic Ice Sheet , 2011, Science.

[56]  Rob Knight,et al.  UCHIME improves sensitivity and speed of chimera detection , 2011, Bioinform..

[57]  J. Pawlowski,et al.  Novel lineages of Southern Ocean deep-sea foraminifera revealed by environmental DNA sequencing , 2011 .

[58]  G. Michel,et al.  Environmental and Gut Bacteroidetes: The Food Connection , 2011, Front. Microbio..

[59]  Susan M. Huse,et al.  Global Patterns of Bacterial Beta-Diversity in Seafloor and Seawater Ecosystems , 2011, PloS one.

[60]  A. Teske,et al.  Archaea in Organic-Lean and Organic-Rich Marine Subsurface Sediments: An Environmental Gradient Reflected in Distinct Phylogenetic Lineages , 2012, Front. Microbio..

[61]  D. DeMaster,et al.  Pelagic-Benthic Coupling, Food Banks, and Climate Change on the West Antarctic Peninsula Shelf , 2012 .

[62]  William A. Walters,et al.  Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms , 2012, The ISME Journal.

[63]  S. Hay,et al.  Resource quality affects carbon cycling in deep-sea sediments , 2012, The ISME Journal.

[64]  Alison S. Waller,et al.  Role for urea in nitrification by polar marine Archaea , 2012, Proceedings of the National Academy of Sciences.

[65]  B. Liljebladh,et al.  Persistent inflow of warm water onto the central Amundsen shelf , 2012 .

[66]  C. Vetriani,et al.  Galenea microaerophila gen. nov., sp. nov., a mesophilic, microaerophilic, chemosynthetic, thiosulfate-oxidizing bacterium isolated from a shallow-water hydrothermal vent. , 2012, International journal of systematic and evolutionary microbiology.

[67]  D. Vaughan,et al.  Antarctic ice-sheet loss driven by basal melting of ice shelves , 2012, Nature.

[68]  K. Edwards,et al.  The Deep, Dark Energy Biosphere: Intraterrestrial Life on Earth , 2012 .

[69]  A. Boetius,et al.  The energy–diversity relationship of complex bacterial communities in Arctic deep-sea sediments , 2011, The ISME Journal.

[70]  C. Lovejoy,et al.  Distribution and Diversity of a Protist Predator Cryothecomonas (Cercozoa) in Arctic Marine Waters , 2012, The Journal of eukaryotic microbiology.

[71]  J. Stark,et al.  Carbon flow and trophic structure of an Antarctic coastal benthic community as determined by δ13C and δ15N , 2012 .

[72]  Ryan A. Lesniewski,et al.  Genome-enabled transcriptomics reveals archaeal populations that drive nitrification in a deep-sea hydrothermal plume , 2012, The ISME Journal.

[73]  W. Smith,et al.  Influence of hydrography on phytoplankton distribution in the Amundsen and Ross Seas, Antarctica , 2012 .

[74]  Eric Rignot,et al.  A Reconciled Estimate of Ice-Sheet Mass Balance , 2012, Science.

[75]  Susan Holmes,et al.  phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data , 2013, PloS one.

[76]  T. Williams,et al.  The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics. , 2013, Environmental microbiology.

[77]  A. Rogers,et al.  Bacterial biodiversity in deep-sea sediments from two regions of contrasting surface water productivity near the Crozet Islands, Southern Ocean , 2013 .

[78]  C. Pedrós-Alió,et al.  Ecology of marine Bacteroidetes: a comparative genomics approach , 2013, The ISME Journal.

[79]  M. R. van den Broeke,et al.  Calving fluxes and basal melt rates of Antarctic ice shelves , 2013, Nature.

[80]  D. Bromwich,et al.  Central West Antarctica among the most rapidly warming regions on Earth , 2013 .

[81]  S. Spring,et al.  Taxonomy and evolution of bacteriochlorophyll a-containing members of the OM60/NOR5 clade of marine gammaproteobacteria: description of Luminiphilus syltensis gen. nov., sp. nov., reclassification of Haliea rubra as Pseudohaliea rubra gen. nov., comb. nov., and emendation of Chromatocurvus halotoler , 2013, BMC Microbiology.

[82]  Sarah L. Westcott,et al.  Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform , 2013, Applied and Environmental Microbiology.

[83]  Pelin Yilmaz,et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools , 2012, Nucleic Acids Res..

[84]  Ricardo Cavicchioli,et al.  Advection shapes Southern Ocean microbial assemblages independent of distance and environment effects , 2013, Nature Communications.

[85]  S. Wakeham,et al.  Bacterial abundance and composition in marine sediments beneath the Ross Ice Shelf, Antarctica , 2013, Geobiology.

[86]  D. Vaughan,et al.  Grounding-line retreat of the West Antarctic Ice Sheet from inner Pine Island Bay , 2013 .

[87]  A. Enrich-Prast,et al.  Microbial diversity and community structure across environmental gradients in Bransfield Strait, Western Antarctic Peninsula , 2014, Front. Microbiol..

[88]  D. Stahl,et al.  Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation , 2014, Proceedings of the National Academy of Sciences.

[89]  M. Könneke,et al.  Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation , 2014, Proceedings of the National Academy of Sciences.

[90]  A. Buma,et al.  Marine archaeal community structure from Potter Cove, Antarctica: high temporal and spatial dominance of the phylum Thaumarchaeota , 2015, Polar Biology.

[91]  R. Amann,et al.  Indications for algae-degrading benthic microbial communities in deep-sea sediments along the Antarctic Polar Front , 2014 .

[92]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[93]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[94]  Haiwei Luo,et al.  Single-cell genomics shedding light on marine Thaumarchaeota diversification , 2014, The ISME Journal.

[95]  H. Ducklow,et al.  Marine bacterial, archaeal and eukaryotic diversity and community structure on the continental shelf of the western Antarctic Peninsula , 2014 .

[96]  J. Xiong,et al.  Response of Bacterioplankton Communities to Cadmium Exposure in Coastal Water Microcosms with High Temporal Variability , 2014, Applied and Environmental Microbiology.

[97]  Otto X. Cordero,et al.  Distinct dissolved organic matter sources induce rapid transcriptional responses in coexisting populations of Prochlorococcus, Pelagibacter and the OM60 clade. , 2014, Environmental microbiology.

[98]  Charles K. Lee,et al.  Influence of soil properties on archaeal diversity and distribution in the McMurdo Dry Valleys, Antarctica. , 2014, FEMS microbiology ecology.

[99]  Yanlu Qiao,et al.  Bacterial and Archaeal Communities in Sediments of the North Chinese Marginal Seas , 2014, Microbial Ecology.

[100]  B. Orcutt,et al.  Abundant Atribacteria in deep marine sediment from the Adélie Basin, Antarctica , 2015, Front. Microbiol..

[101]  High-Throughput Methods for Ion Channels , 2015 .

[102]  Tan T. Nguyen,et al.  Polar front associated variation in prokaryotic community structure in Arctic shelf seafloor , 2015, Front. Microbiol..

[103]  J. Fuhrman,et al.  Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. , 2016, Environmental microbiology.