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

Abstract

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 aremore » 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.« less

Authors:
ORCiD logo [1]; ORCiD logo [1];  [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [5]; ORCiD logo [6]; ORCiD logo [7]; ORCiD logo [8]; ORCiD logo [8]; ORCiD logo [7]; ORCiD logo [8]; ORCiD logo [9]; ORCiD logo [10]; ORCiD logo [10]
  1. Portland State Univ., OR (United States)
  2. California State Univ. (CalState), Northridge, CA (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. Royal Netherlands Inst. for Sea Research, Den Burg (Netherlands)
  5. Royal Netherlands Inst. for Sea Research, Den Burg (Netherlands); Uppsala Univ. (Sweden)
  6. Univ. de Bretagne Occidentale, Plouzané (France)
  7. Woods Hole Oceanographic Institution, Woods Hole, MA (United States)
  8. GNS Science, Avalon (New Zealand)
  9. GNS Science, Avalon (New Zealand); Toha Science, Wellington (New Zealand)
  10. Univ. of Bremen (Germany)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE; National Science Foundation (NSF); Swedish Research Council (SRC)
OSTI Identifier:
1755295
Grant/Contract Number:  
AC05-00OR22725; OCE‐1558356; OCE-1558795; 2016-03559
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 117; Journal Issue: 51; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; metagenomics; deep-sea hydrothermal; thermophiles; Archaea; volcanics

Citation Formats

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, and Bach, Wolfgang. Complex subsurface hydrothermal fluid mixing at a submarine arc volcano supports distinct and highly diverse microbial communities. United States: N. p., 2020. Web. https://doi.org/10.1073/pnas.2019021117.
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. Complex subsurface hydrothermal fluid mixing at a submarine arc volcano supports distinct and highly diverse microbial communities. United States. https://doi.org/10.1073/pnas.2019021117
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, and Bach, Wolfgang. Fri . "Complex subsurface hydrothermal fluid mixing at a submarine arc volcano supports distinct and highly diverse microbial communities". United States. https://doi.org/10.1073/pnas.2019021117. https://www.osti.gov/servlets/purl/1755295.
@article{osti_1755295,
title = {Complex subsurface hydrothermal fluid mixing at a submarine arc volcano supports distinct and highly diverse microbial communities},
author = {Reysenbach, Anna-Louise and St. John, Emily and Meneghin, Jennifer and Flores, Gilberto E. and Podar, Mircea and Dombrowski, Nina and Spang, Anja and L’Haridon, Stephane and Humphris, Susan E. and de Ronde, Cornel J. and Caratori Tontini, Fabio and Tivey, Maurice and Stucker, Valerie K. and Stewart, Lucy C. and Diehl, Alexander and Bach, Wolfgang},
abstractNote = {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.},
doi = {10.1073/pnas.2019021117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 51,
volume = 117,
place = {United States},
year = {2020},
month = {12}
}

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