Tectonic and geological setting influence hot spring microbiology

Daniel R. Colman; Allison Veach; Andri Stefánsson; Louie Wurch; B. Shafer Belisle; Peter T. Podar; Zamin Yang; Dawn Klingeman; Kazuyo Senba; Katsuhiko S. Murakami; Jakob K. Kristjánsson; Snædís H. Björnsdóttir; Eric S. Boyd; Mircea Podar

doi:10.1111/1462-2920.16472

Tectonic and geological setting influence hot spring microbiology

Daniel R. Colman, Allison Veach, Andri Stefánsson, Louie Wurch, B. Shafer Belisle, Peter T. Podar, Zamin Yang, Dawn Klingeman, Kazuyo Senba, Katsuhiko S. Murakami, Jakob K. Kristjánsson, Snædís H. Björnsdóttir, Eric S. Boyd, Mircea Podar

Research output: Contribution to journal › Article › peer-review

3 Scopus citations

Abstract

Hydrothermal systems form at divergent and convergent boundaries of lithospheric plates and within plates due to weakened crust and mantle plumes, playing host to diverse microbial ecosystems. Little is known of how differences in tectonic setting influence the geochemical and microbial compositions of these hydrothermal ecosystems. Here, coordinated geochemical and microbial community analyses were conducted on 87 high-temperature (>65°C) water and sediment samples from hot springs in Yellowstone National Park, Wyoming, USA (n = 41; mantle plume setting), Iceland (n = 41, divergent boundary), and Japan (n = 5; convergent boundary). Region-specific variation in geochemistry and sediment-associated 16S rRNA gene amplicon sequence variant (ASV) composition was observed, with 16S rRNA gene assemblages being nearly completely distinguished by region and pH being the most explanatory parameter within regions. Several low abundance ASVs exhibited cosmopolitan distributions across regions, while most high-abundance ASVs were only identified in specific regions. The presence of some cosmopolitan ASVs across regions argues against dispersal limitation primarily shaping the distribution of taxa among regions. Rather, the results point to local tectonic and geologic characteristics shaping the geochemistry of continental hydrothermal systems that then select for distinct microbial assemblages. These results provide new insights into the co-evolution of hydrothermal systems and their microbial communities.

Original language	English
Pages (from-to)	2481-2497
Number of pages	17
Journal	Environmental Microbiology
Volume	25
Issue number	11
DOIs	https://doi.org/10.1111/1462-2920.16472
State	Published - Nov 2023

Funding

Field and laboratory work in the M.P. lab was supported by grants from the U.S. Department of Energy (DOE-BER, DE-SC0006654), National Science Foundation (DEB1134877) and NASA (NNX16AJ66G). The Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the U.S. Department of Energy under contract DE-AC05-00OR22725. Sampling in Yellowstone National Park was conducted under permit YELL-2008-SCI-5714 and we thank the YNP administration for logistical support. Sampling in Iceland was conducted under permits issued by Iceland's National Energy Authority (Orkustofnun) to Mircea Podar and Snædís H. Björnsdóttir. We thank the Beppu Onsen association for permission to sample hot springs in Beppu, Japan. We thank Adrian Gonzalez from The University of Tennessee Knoxville Water Quality Core Facility for chemical analysis of the water samples and other colleagues for assistance with sampling and sample processing. Daniel R. Colman and Eric S. Boyd acknowledge support from NASA (80NSSC19M0150). Field and laboratory work in the M.P. lab was supported by grants from the U.S. Department of Energy (DOE‐BER, DE‐SC0006654), National Science Foundation (DEB1134877) and NASA (NNX16AJ66G). The Oak Ridge National Laboratory is managed by UT‐Battelle, LLC, for the U.S. Department of Energy under contract DE‐AC05‐00OR22725. Sampling in Yellowstone National Park was conducted under permit YELL‐2008‐SCI‐5714 and we thank the YNP administration for logistical support. Sampling in Iceland was conducted under permits issued by Iceland's National Energy Authority (Orkustofnun) to Mircea Podar and Snædís H. Björnsdóttir. We thank the Beppu Onsen association for permission to sample hot springs in Beppu, Japan. We thank Adrian Gonzalez from The University of Tennessee Knoxville Water Quality Core Facility for chemical analysis of the water samples and other colleagues for assistance with sampling and sample processing. Daniel R. Colman and Eric S. Boyd acknowledge support from NASA (80NSSC19M0150).

Funders	Funder number
DOE-BER	DE-SC0006654
University of Tennessee Knoxville Water Quality Core Facility
National Science Foundation	DEB1134877
U.S. Department of Energy	DE‐SC0006654
National Aeronautics and Space Administration	NNX16AJ66G
Oak Ridge National Laboratory	DE‐AC05‐00OR22725, 80NSSC19M0150

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10.1111/1462-2920.16472

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title = "Tectonic and geological setting influence hot spring microbiology",

abstract = "Hydrothermal systems form at divergent and convergent boundaries of lithospheric plates and within plates due to weakened crust and mantle plumes, playing host to diverse microbial ecosystems. Little is known of how differences in tectonic setting influence the geochemical and microbial compositions of these hydrothermal ecosystems. Here, coordinated geochemical and microbial community analyses were conducted on 87 high-temperature (>65°C) water and sediment samples from hot springs in Yellowstone National Park, Wyoming, USA (n = 41; mantle plume setting), Iceland (n = 41, divergent boundary), and Japan (n = 5; convergent boundary). Region-specific variation in geochemistry and sediment-associated 16S rRNA gene amplicon sequence variant (ASV) composition was observed, with 16S rRNA gene assemblages being nearly completely distinguished by region and pH being the most explanatory parameter within regions. Several low abundance ASVs exhibited cosmopolitan distributions across regions, while most high-abundance ASVs were only identified in specific regions. The presence of some cosmopolitan ASVs across regions argues against dispersal limitation primarily shaping the distribution of taxa among regions. Rather, the results point to local tectonic and geologic characteristics shaping the geochemistry of continental hydrothermal systems that then select for distinct microbial assemblages. These results provide new insights into the co-evolution of hydrothermal systems and their microbial communities.",

author = "Colman, {Daniel R.} and Allison Veach and Andri Stef{\'a}nsson and Louie Wurch and Belisle, {B. Shafer} and Podar, {Peter T.} and Zamin Yang and Dawn Klingeman and Kazuyo Senba and Murakami, {Katsuhiko S.} and Kristj{\'a}nsson, {Jakob K.} and Bj{\"o}rnsd{\'o}ttir, {Sn{\ae}d{\'i}s H.} and Boyd, {Eric S.} and Mircea Podar",

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AU - Colman, Daniel R.

AU - Veach, Allison

AU - Stefánsson, Andri

AU - Wurch, Louie

AU - Belisle, B. Shafer

AU - Podar, Peter T.

AU - Yang, Zamin

AU - Klingeman, Dawn

AU - Senba, Kazuyo

AU - Murakami, Katsuhiko S.

AU - Kristjánsson, Jakob K.

AU - Björnsdóttir, Snædís H.

AU - Boyd, Eric S.

AU - Podar, Mircea

PY - 2023/11

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AB - Hydrothermal systems form at divergent and convergent boundaries of lithospheric plates and within plates due to weakened crust and mantle plumes, playing host to diverse microbial ecosystems. Little is known of how differences in tectonic setting influence the geochemical and microbial compositions of these hydrothermal ecosystems. Here, coordinated geochemical and microbial community analyses were conducted on 87 high-temperature (>65°C) water and sediment samples from hot springs in Yellowstone National Park, Wyoming, USA (n = 41; mantle plume setting), Iceland (n = 41, divergent boundary), and Japan (n = 5; convergent boundary). Region-specific variation in geochemistry and sediment-associated 16S rRNA gene amplicon sequence variant (ASV) composition was observed, with 16S rRNA gene assemblages being nearly completely distinguished by region and pH being the most explanatory parameter within regions. Several low abundance ASVs exhibited cosmopolitan distributions across regions, while most high-abundance ASVs were only identified in specific regions. The presence of some cosmopolitan ASVs across regions argues against dispersal limitation primarily shaping the distribution of taxa among regions. Rather, the results point to local tectonic and geologic characteristics shaping the geochemistry of continental hydrothermal systems that then select for distinct microbial assemblages. These results provide new insights into the co-evolution of hydrothermal systems and their microbial communities.

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Tectonic and geological setting influence hot spring microbiology

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