Complex subsurface hydrothermal fluid mixing at a submarine arc volcano supports distinct and highly diverse microbial communities

Reysenbach, Anna-Louise; St. John, Emily; Meneghin, Jennifer; Flores, Gilberto E.; Podar, Mircea; Dombrowski, Nina; Spang, Anja; L’Haridon, Stephane; Humphris, Susan E.; de Ronde, Cornel J.; Caratori Tontini, Fabio; Tivey, Maurice; Stucker, Valerie K.; Stewart, Lucy C.; Diehl, Alexander; Bach, Wolfgang

doi:10.1073/pnas.2019021117

Title: Complex subsurface hydrothermal fluid mixing at a submarine arc volcano supports distinct and highly diverse microbial communities

Journal Article · 04 December 2020 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.2019021117 · OSTI ID:1755295

^[1];

^[1]; Meneghin, Jennifer ^[1];

^[2];

^[3];

^[4];

^[5];

^[6];

^[7];

^[8];

^[7];

^[8];

^[9];

^[10];

^[10]

Portland State Univ., OR (United States)
California State Univ. (CalState), Northridge, CA (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Royal Netherlands Inst. for Sea Research, Den Burg (Netherlands)
Royal Netherlands Inst. for Sea Research, Den Burg (Netherlands); Uppsala Univ. (Sweden)
Univ. de Bretagne Occidentale, Plouzané (France)
Woods Hole Oceanographic Institution, Woods Hole, MA (United States)
GNS Science, Avalon (New Zealand)
GNS Science, Avalon (New Zealand); Toha Science, Wellington (New Zealand)
Univ. of Bremen (Germany)

Hydrothermally active submarine volcanoes are mineral-rich biological oases contributing significantly to chemical fluxes in the deep sea, yet little is known about the microbial communities inhabiting these systems. Here we investigate the diversity of microbial life in hydrothermal deposits and their metagenomics-inferred physiology in light of the geological history and resulting hydrothermal fluid paths in the subsurface of Brothers submarine volcano north of New Zealand on the southern Kermadec arc. From metagenome-assembled genomes we identified over 90 putative bacterial and archaeal genomic families and nearly 300 previously unknown genera, many potentially endemic to this submarine volcanic environment. While magmatically influenced hydrothermal systems on the volcanic resurgent cones of Brothers volcano harbor communities of thermoacidophiles and diverse members of the superphylum “DPANN,” two distinct communities are associated with the caldera wall, likely shaped by two different types of hydrothermal circulation. The communities whose phylogenetic diversity primarily aligns with that of the cone sites and magmatically influenced hydrothermal systems elsewhere are characterized predominately by anaerobic metabolisms. These populations are probably maintained by fluids with greater magmatic inputs that have interacted with different (deeper) previously altered mineral assemblages. However, proximal (a few meters distant) communities with gene-inferred aerobic, microaerophilic, and anaerobic metabolisms are likely supported by shallower seawater-dominated circulation. Furthermore, mixing of fluids from these two distinct hydrothermal circulation systems may have an underlying imprint on the high microbial phylogenomic diversity. Collectively our results highlight the importance of considering geologic evolution and history of subsurface processes in studying microbial colonization and community dynamics in volcanic environments.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE; National Science Foundation (NSF); Swedish Research Council (SRC)

Grant/Contract Number:: AC05-00OR22725; OCE‐1558356; OCE-1558795; 2016-03559

OSTI ID:: 1755295

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 117, Issue 51; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (67)

A new gas-tight isobaric sampler for hydrothermal fluids Seewald, Jeffrey S.; Doherty, Kenneth W.; Hammar, Terence R. Deep Sea Research Part I: Oceanographic Research Papers, Vol. 49, Issue 1 https://doi.org/10.1016/S0967-0637(01)00046-2	journal	January 2002
Culture-independent characterization of a novel microbial community at a hydrothermal vent at Brothers volcano, Kermadec arc, New Zealand: MICROBIAL ECOLOGY OF BROTHERS SEAMOUNT Stott, M. B.; Saito, J. A.; Crowe, M. A. Journal of Geophysical Research: Solid Earth, Vol. 113, Issue B8 https://doi.org/10.1029/2007JB005477	journal	August 2008
Asgard archaea illuminate the origin of eukaryotic cellular complexity Zaremba-Niedzwiedzka, Katarzyna; Caceres, Eva F.; Saw, Jimmy H. Nature, Vol. 541, Issue 7637 https://doi.org/10.1038/nature21031	journal	January 2017
Microbial community dynamics in Inferno Crater Lake, a thermally fluctuating geothermal spring Ward, Laura; Taylor, Michael W.; Power, Jean F. The ISME Journal, Vol. 11, Issue 5 https://doi.org/10.1038/ismej.2016.193	journal	January 2017
The Intersection of Geology, Geochemistry, and Microbiology in Continental Hydrothermal Systems Colman, Daniel R.; Lindsay, Melody R.; Amenabar, Maximiliano J. Astrobiology, Vol. 19, Issue 12 https://doi.org/10.1089/ast.2018.2016	journal	December 2019
Mixing of meteoric and geothermal fluids supports hyperdiverse chemosynthetic hydrothermal communities Colman, Daniel R.; Lindsay, Melody R.; Boyd, Eric S. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08499-1	journal	February 2019
Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea Bowers, Robert M.; Kyrpides, Nikos C.; Stepanauskas, Ramunas Nature Biotechnology, Vol. 35, Issue 8 https://doi.org/10.1038/nbt.3893	journal	August 2017
Geochemistry and Dynamics of the Yellowstone National Park Hydrothermal System Fournier, R. O. Annual Review of Earth and Planetary Sciences, Vol. 17, Issue 1 https://doi.org/10.1146/annurev.ea.17.050189.000305	journal	May 1989
Archaeal Clusters of Orthologous Genes (arCOGs): An Update and Application for Analysis of Shared Features between Thermococcales, Methanococcales, and Methanobacteriales Makarova, Kira; Wolf, Yuri; Koonin, Eugene Life, Vol. 5, Issue 1 https://doi.org/10.3390/life5010818	journal	March 2015
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
Geologic legacy spanning >90 years explains unique Yellowstone hot spring geochemistry and biodiversity Payne, Devon; Dunham, Eric C.; Mohr, Elizabeth Environmental Microbiology, Vol. 21, Issue 11 https://doi.org/10.1111/1462-2920.14775	journal	August 2019
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Community-wide analysis of microbial genome sequence signatures Dick, Gregory J.; Andersson, Anders F.; Baker, Brett J. Genome Biology, Vol. 10, Issue 8 https://doi.org/10.1186/gb-2009-10-8-r85	journal	January 2009
Geochemistry of hydrothermal fluids from the PACMANUS, Northeast Pual and Vienna Woods hydrothermal fields, Manus Basin, Papua New Guinea Reeves, Eoghan P.; Seewald, Jeffrey S.; Saccocia, Peter Geochimica et Cosmochimica Acta, Vol. 75, Issue 4 https://doi.org/10.1016/j.gca.2010.11.008	journal	February 2011
Variable morphologic expression of volcanic, tectonic, and hydrothermal processes at six hydrothermal vent fields in the Lau back-arc basin: HYDROTHERMAL PROCESSES IN LAU BACK-ARC BASIN Ferrini, Vicki Lynn; Tivey, Margaret K.; Carbotte, Suzanne M. Geochemistry, Geophysics, Geosystems, Vol. 9, Issue 7 https://doi.org/10.1029/2008GC002047	journal	July 2008
Geochemical characterization of highly diverse hydrothermal fluids from volcanic vent systems of the Kermadec intraoceanic arc Kleint, Charlotte; Bach, Wolfgang; Diehl, Alexander Chemical Geology, Vol. 528 https://doi.org/10.1016/j.chemgeo.2019.119289	journal	December 2019
Submarine hydrothermal activity and gold-rich mineralization at Brothers Volcano, Kermadec Arc, New Zealand de Ronde, Cornel E. J.; Massoth, Gary J.; Butterfield, David A. Mineralium Deposita, Vol. 46, Issue 5-6 https://doi.org/10.1007/s00126-011-0345-8	journal	May 2011
Sulfur Metabolisms in Epsilon- and Gamma-Proteobacteria in Deep-Sea Hydrothermal Fields Yamamoto, Masahiro; Takai, Ken Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00192	journal	January 2011
BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences Kanehisa, Minoru; Sato, Yoko; Morishima, Kanae Journal of Molecular Biology, Vol. 428, Issue 4 https://doi.org/10.1016/j.jmb.2015.11.006	journal	February 2016
metaSPAdes: a new versatile metagenomic assembler Nurk, Sergey; Meleshko, Dmitry; Korobeynikov, Anton Genome Research, Vol. 27, Issue 5 https://doi.org/10.1101/gr.213959.116	journal	March 2017
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities Kang, Dongwan D.; Froula, Jeff; Egan, Rob PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1165	journal	January 2015
Large-scale differences in microbial biodiversity discovery between 16S amplicon and shotgun sequencing Tessler, Michael; Neumann, Johannes S.; Afshinnekoo, Ebrahim Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-06665-3	journal	July 2017
BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments Criscuolo, Alexis; Gribaldo, Simonetta BMC Evolutionary Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2148-10-210	journal	January 2010
Deblur Rapidly Resolves Single-Nucleotide Community Sequence Patterns Amir, Amnon; McDonald, Daniel; Navas-Molina, Jose A. mSystems, Vol. 2, Issue 2 https://doi.org/10.1128/mSystems.00191-16	journal	March 2017
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
Kīlauea lava fuels phytoplankton bloom in the North Pacific Ocean Wilson, Samuel T.; Hawco, Nicholas J.; Armbrust, E. Virginia Science, Vol. 365, Issue 6457 https://doi.org/10.1126/science.aax4767	journal	September 2019
A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data Li, H. Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr509	journal	September 2011
MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices Li, Dinghua; Luo, Ruibang; Liu, Chi-Man Methods, Vol. 102 https://doi.org/10.1016/j.ymeth.2016.02.020	journal	June 2016
Critical role of caldera collapse in the formation of seafloor mineralization: The case of Brothers volcano de Ronde, Cornel E. J.; Humphris, Susan E.; Höfig, Tobias W. Geology, Vol. 47, Issue 8 https://doi.org/10.1130/G46047.1	journal	June 2019
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
Heat Flow and Near‐Seafloor Magnetic Anomalies Highlight Hydrothermal Circulation at Brothers Volcano Caldera, Southern Kermadec Arc, New Zealand Caratori Tontini, F.; Tivey, M. A.; Ronde, C. E. J. Geophysical Research Letters, Vol. 46, Issue 14 https://doi.org/10.1029/2019GL083517	journal	July 2019
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Prokka: rapid prokaryotic genome annotation Seemann, T. Bioinformatics, Vol. 30, Issue 14 https://doi.org/10.1093/bioinformatics/btu153	journal	March 2014
Chemistry of submarine hydrothermal solutions at 21 °N, East Pacific Rise Von Damm, K. L.; Edmond, J. M.; Grant, B. Geochimica et Cosmochimica Acta, Vol. 49, Issue 11 https://doi.org/10.1016/0016-7037(85)90222-4	journal	November 1985
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Inter-field variability in the microbial communities of hydrothermal vent deposits from a back-arc basin: Microbial communities of hydrothermal deposits Flores, G. E.; Shakya, M.; Meneghin, J. Geobiology, Vol. 10, Issue 4 https://doi.org/10.1111/j.1472-4669.2012.00325.x	journal	March 2012
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform Katoh, K. Nucleic Acids Research, Vol. 30, Issue 14 https://doi.org/10.1093/nar/gkf436	journal	July 2002
Shallow breathing: bacterial life at low O2 Morris, Rachel L.; Schmidt, Thomas M. Nature Reviews Microbiology, Vol. 11, Issue 3 https://doi.org/10.1038/nrmicro2970	journal	February 2013
Volcanic calderas delineate biogeographic provinces among Yellowstone thermophiles Takacs-Vesbach, Cristina; Mitchell, Kendra; Jackson-Weaver, Olan Environmental Microbiology, Vol. 10, Issue 7 https://doi.org/10.1111/j.1462-2920.2008.01584.x	journal	July 2008
HydDB: A web tool for hydrogenase classification and analysis Søndergaard, Dan; Pedersen, Christian N. S.; Greening, Chris Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep34212	journal	September 2016
Links from Mantle to Microbe at the Lau Integrated Study Site: Insights from a Back-Arc Spreading Center Tivey, Margaret; Becker, Erin; Beinart, Roxanne Oceanography, Vol. 25, Issue 1 https://doi.org/10.5670/oceanog.2012.04	journal	March 2012
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 Bolyen, Evan; Rideout, Jai Ram; Dillon, Matthew R. Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0209-9	journal	July 2019
Variability in microbial community and venting chemistry in a sediment-hosted backarc hydrothermal system: Impacts of subseafloor phase-separation Nakagawa, Satoshi; Takai, Ken; Inagaki, Fumio FEMS Microbiology Ecology, Vol. 54, Issue 1 https://doi.org/10.1016/j.femsec.2005.03.007	journal	September 2005
Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples: Primers for marine microbiome studies Parada, Alma E.; Needham, David M.; Fuhrman, Jed A. Environmental Microbiology, Vol. 18, Issue 5 https://doi.org/10.1111/1462-2920.13023	journal	October 2015
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Mineralogy and Formation of Black Smoker Chimneys from Brothers Submarine Volcano, Kermadec Arc Berkenbosch, H. A.; de Ronde, C. E. J.; Gemmell, J. B. Economic Geology, Vol. 107, Issue 8 https://doi.org/10.2113/econgeo.107.8.1613	journal	November 2012
A new view of the tree of life Hug, Laura A.; Baker, Brett J.; Anantharaman, Karthik Nature Microbiology, Vol. 1, Issue 5 https://doi.org/10.1038/nmicrobiol.2016.48	journal	April 2016
Catabolic and anabolic energy for chemolithoautotrophs in deep-sea hydrothermal systems hosted in different rock types Amend, Jan P.; McCollom, Thomas M.; Hentscher, Michael Geochimica et Cosmochimica Acta, Vol. 75, Issue 19 https://doi.org/10.1016/j.gca.2011.07.041	journal	October 2011
Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts Fan, L.; Reynolds, D.; Liu, M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 27 https://doi.org/10.1073/pnas.1203287109	journal	June 2012
Genome‐resolved metagenomics and metatranscriptomics reveal niche differentiation in functionally redundant microbial communities at deep‐sea hydrothermal vents Galambos, David; Anderson, Rika E.; Reveillaud, Julie Environmental Microbiology, Vol. 21, Issue 11 https://doi.org/10.1111/1462-2920.14806	journal	October 2019
Variability in Microbial Communities in Black Smoker Chimneys at the NW Caldera Vent Field, Brothers Volcano, Kermadec Arc Takai, Ken; Nunoura, Takuro; Horikoshi, Koki Geomicrobiology Journal, Vol. 26, Issue 8 https://doi.org/10.1080/01490450903304949	journal	November 2009
Evolution of a Submarine Magmatic-Hydrothermal System: Brothers Volcano, Southern Kermadec Arc, New Zealand de Ronde, C. E. J.; Hannington, M. D.; Stoffers, P. Economic Geology, Vol. 100, Issue 6 https://doi.org/10.2113/gsecongeo.100.6.1097	journal	September 2005
Comparative Genomic Analysis of the Class Epsilonproteobacteria and Proposed Reclassification to Epsilonbacteraeota (phyl. nov.) Waite, David W.; Vanwonterghem, Inka; Rinke, Christian Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00682	journal	April 2017
PhyloSift: phylogenetic analysis of genomes and metagenomes Darling, Aaron E.; Jospin, Guillaume; Lowe, Eric PeerJ, Vol. 2 https://doi.org/10.7717/peerj.243	journal	January 2014
Rates of magma emplacement and volcanic output Crisp, Joy A. Journal of Volcanology and Geothermal Research, Vol. 20, Issue 3-4 https://doi.org/10.1016/0377-0273(84)90039-8	journal	April 1984
Interactive Tree Of Life (iTOL) v4: recent updates and new developments Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 47, Issue W1 https://doi.org/10.1093/nar/gkz239	journal	April 2019
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13219	journal	October 2016
The abundance of seafloor massive sulfide deposits Hannington, M.; Jamieson, J.; Monecke, T. Geology, Vol. 39, Issue 12 https://doi.org/10.1130/G32468.1	journal	October 2011
Individual hydrothermal vents at Axial Seamount harbor distinct subseafloor microbial communities Opatkiewicz, Andrew D.; Butterfield, David A.; Baross, John A. FEMS Microbiology Ecology, Vol. 70, Issue 3 https://doi.org/10.1111/j.1574-6941.2009.00747.x	journal	December 2009
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Superoxide Dismutases and Superoxide Reductases Sheng, Yuewei; Abreu, Isabel A.; Cabelli, Diane E. Chemical Reviews, Vol. 114, Issue 7 https://doi.org/10.1021/cr4005296	journal	January 2014
FeGenie: A Comprehensive Tool for the Identification of Iron Genes and Iron Gene Neighborhoods in Genome and Metagenome Assemblies Garber, Arkadiy I.; Nealson, Kenneth H.; Okamoto, Akihiro Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.00037	journal	January 2020
Ecological Aspects of the Distribution of Different Autotrophic CO ₂ Fixation Pathways Berg, Ivan A. Applied and Environmental Microbiology, Vol. 77, Issue 6 https://doi.org/10.1128/AEM.02473-10	journal	January 2011
Genomic variation in microbial populations inhabiting the marine subseafloor at deep-sea hydrothermal vents Anderson, Rika E.; Reveillaud, Julie; Reddington, Emily Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01228-6	journal	October 2017
GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database Chaumeil, Pierre-Alain; Mussig, Aaron J.; Hugenholtz, Philip Bioinformatics https://doi.org/10.1093/bioinformatics/btz848	journal	November 2019

Cited By (1)

Additional file 1 of Sulfur-cycling chemolithoautotrophic microbial community dominates a cold, anoxic, hypersaline Arctic spring Magnuson, Elisse; Altshuler, Ianina; Freyria, Nastasia J. figshare https://doi.org/10.6084/m9.figshare.24123771.v1	dataset	January 2023

Similar Records

Global patterns of diversity and metabolism of microbial communities in deep-sea hydrothermal vent deposits

Journal Article · 2022 · Microbiome · OSTI ID:2422816

Zhou, Zhichao; St. John, Emily; Anantharaman, Karthik; +1 more

Genomic expansion of Domain Archaea highlights roles for organisms from new phyla in anaerobic carbon cycling

Journal Article · 2015 · Current Biology, 25(6):690-701 · OSTI ID:1184900

Castelle, Cindy; Wrighton, Kelly C.; Thomas, Brian C.; +10 more

Brockarchaeota, a novel archaeal phylum with unique and versatile carbon cycling pathways

Journal Article · 2021 · Nature Communications · OSTI ID:1816313

De Anda, Valerie; Chen, Lin-Xing; Dombrowski, Nina; +5 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
metagenomics
deep-sea hydrothermal
thermophiles
Archaea
volcanics

Title: Complex subsurface hydrothermal fluid mixing at a submarine arc volcano supports distinct and highly diverse microbial communities

Citation Formats

References (67)

Cited By (1)

Linked Research (1)

Similar Records

Related Subjects