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

Type Article
Date 2020-12
Language English
Author(s) Reysenbach Anna-Louise1, St John Emily1, Meneghin Jennifer1, Flores Gilberto E.2, Podar Mircea3, Dombrowski NinaORCID4, Spang AnjaORCID4, 5, L'Haridon Stephane6, Humphris Susan E.7, de Ronde Cornel E. J.8, Tontini Fabio Caratori8, Tivey Maurice7, Stucker Valerie K.9, Stewart Lucy C.8, 10, Diehl AlexanderORCID11, 12, Bach Wolfgang11, 12
Affiliation(s) 1 : Portland State Univ, Ctr Life Extreme Environm, Biol Dept, Portland, OR 97201, USA.
2 : Calif State Univ Northridge, Dept Biol, Northridge, CA 91330, USA.
3 : Oak Ridge Natl Lab, Biosci Div, POB 2009, Oak Ridge, TN 37831, USA.
4 : Royal Netherlands Inst Sea Res, Dept Marine Microbiol & Biogeochem, NL-1790 AB Den Burg, Netherlands.
5 : Uppsala Univ, Dept Cell & Mol Biol, Sci Life Lab, SE-75123 Uppsala, Sweden.
6 : Univ Bretagne Occident, Lab Microbiol Environm Extremes, CNRS, Inst Francais Rech Exploitat Mer, F-29280 Plouzane, France.
7 : Woods Hole Oceanog Inst, Dept Geol & Geophys, Woods Hole, MA 02543, USA.
8 : GNS Sci, Dept Earth Syst & Resources, Lower Hutt 5010, New Zealand.
9 : GNS Sci, Labs & Collect, Lower Hutt 5010, New Zealand.
10 : Toha Sci, Wellington 6011, New Zealand.
11 : Univ Bremen, Fac Geosci, D-28359 Bremen, Germany.
12 : Univ Bremen, MARUM Ctr Marine Environm Sci, D-28359 Bremen, Germany.
Source Proceedings Of The National Academy Of Sciences Of The United States Of America (0027-8424) (Natl Acad Sciences), 2020-12 , Vol. 117 , N. 51 , P. 32627-32638
DOI 10.1073/pnas.2019021117
WOS© Times Cited 5
Keyword(s) metagenomics, deep-sea hydrothermal, thermophiles, Archaea, volcanics
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 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.
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Publisher's official version 12 1 MB Open access
Appendix 34 9 MB Open access
Dataset S01 116 KB Open access
Dataset S02 44 KB Open access
Dataset S03 390 KB Open access
Dataset S04 47 KB Open access
Dataset S05 31 KB Open access
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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 E. J., Tontini Fabio Caratori, Tivey Maurice, Stucker Valerie K., Stewart Lucy C., Diehl Alexander, Bach Wolfgang (2020). Complex subsurface hydrothermal fluid mixing at a submarine arc volcano supports distinct and highly diverse microbial communities. Proceedings Of The National Academy Of Sciences Of The United States Of America, 117(51), 32627-32638. Publisher's official version : https://doi.org/10.1073/pnas.2019021117 , Open Access version : https://archimer.ifremer.fr/doc/00668/78035/