Microbial community differentiation in vent chimneys of the Lost City Hydrothermal Field reflects habitat heterogeneity

Oceanic hydrothermal vent systems represent some of the oldest habitats on Earth and serve as analogs for extraterrestrial environments. The Lost City Hydrothermal Field (LCHF) near the Mid-Atlantic Ridge is one such environment, and its large chimneys are unique in hosting actively venting hydrothe...

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Main Authors: Osama M. Alian, William J. Brazelton, Karmina A. Aquino, Katrina I. Twing, H. Lizethe Pendleton, Gretchen Früh-Green, Susan Q. Lang, Matthew O. Schrenk
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Microbiomes
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Online Access:https://www.frontiersin.org/articles/10.3389/frmbi.2024.1401831/full
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author Osama M. Alian
William J. Brazelton
Karmina A. Aquino
Katrina I. Twing
H. Lizethe Pendleton
Gretchen Früh-Green
Susan Q. Lang
Matthew O. Schrenk
Matthew O. Schrenk
author_facet Osama M. Alian
William J. Brazelton
Karmina A. Aquino
Katrina I. Twing
H. Lizethe Pendleton
Gretchen Früh-Green
Susan Q. Lang
Matthew O. Schrenk
Matthew O. Schrenk
author_sort Osama M. Alian
collection DOAJ
description Oceanic hydrothermal vent systems represent some of the oldest habitats on Earth and serve as analogs for extraterrestrial environments. The Lost City Hydrothermal Field (LCHF) near the Mid-Atlantic Ridge is one such environment, and its large chimneys are unique in hosting actively venting hydrothermal fluids that are primarily controlled by serpentinization reactions in the subseafloor. Microbial communities within LCHF have been studied for insights into their functional adaptations to the warm, alkaline, and dissolved inorganic carbon-limited environment. Metagenomic and mineralogical data collected during a recent expedition to Lost City were analyzed to delineate associations between microbial populations and physical, chemical and biological characteristics of the chimneys. Bacterial 16S rRNA gene sequences show a high degree of putative microdiversity within the relatively dominant genera Desulfotomaculum, Sulfurovum, Thiomicrorhabdus, and Serpentinicella, which represent a large core of the overall LCHF vent bacterial community. This microdiversity relates to the compositional fraction of aragonite, brucite, and calcite minerals within chimney samples rather than just the composition of nearby vent fluids. Although many species are found in both chimneys and venting fluids, the overall microbial community structures in chimney biofilms remain distinct from the hydrothermal fluids that flow through them. Shotgun metagenomic analyses reveal differences among genes predicted to be involved in carbon, methane, nitrogen and sulfur cycling with respect to their correlations to the abundances of specific minerals. These data hint at microenvironmental complexity lost within standard bulk analyses. The findings of this study underscore the need to more closely examine microbe-mineral interactions in natural environments, critically informing not just population-level distributions, but also the functional underpinnings of these extremophile microbial communities.
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spelling doaj-art-fa0cd064ed48401f83048b6f94cd709a2025-01-20T07:20:34ZengFrontiers Media S.A.Frontiers in Microbiomes2813-43382025-01-01310.3389/frmbi.2024.14018311401831Microbial community differentiation in vent chimneys of the Lost City Hydrothermal Field reflects habitat heterogeneityOsama M. Alian0William J. Brazelton1Karmina A. Aquino2Katrina I. Twing3H. Lizethe Pendleton4Gretchen Früh-Green5Susan Q. Lang6Matthew O. Schrenk7Matthew O. Schrenk8Department of Microbiology, Genetics, and Immunology, Michigan State University, East Lansing, MI, United StatesSchool of Biological Sciences, University of Utah, Salt Lake City, UT, United StatesDepartment of Science and Technology - Philippine Nuclear Research Institute, Quezon City, PhilippinesDepartment of Microbiology, Weber State University, Ogden, UT, United StatesSchool of Biological Sciences, University of Utah, Salt Lake City, UT, United StatesDepartment of Earth Sciences, Eidgenössiche Technische Hochschule Zürich, Zürich, SwitzerlandDepartment of Geology and Geophysics, Woods Hole Oceanographic Institution, Woods Hole, MA, United StatesDepartment of Microbiology, Genetics, and Immunology, Michigan State University, East Lansing, MI, United StatesDepartment of Earth and Environmental Science, Michigan State University, East Lansing, MI, United StatesOceanic hydrothermal vent systems represent some of the oldest habitats on Earth and serve as analogs for extraterrestrial environments. The Lost City Hydrothermal Field (LCHF) near the Mid-Atlantic Ridge is one such environment, and its large chimneys are unique in hosting actively venting hydrothermal fluids that are primarily controlled by serpentinization reactions in the subseafloor. Microbial communities within LCHF have been studied for insights into their functional adaptations to the warm, alkaline, and dissolved inorganic carbon-limited environment. Metagenomic and mineralogical data collected during a recent expedition to Lost City were analyzed to delineate associations between microbial populations and physical, chemical and biological characteristics of the chimneys. Bacterial 16S rRNA gene sequences show a high degree of putative microdiversity within the relatively dominant genera Desulfotomaculum, Sulfurovum, Thiomicrorhabdus, and Serpentinicella, which represent a large core of the overall LCHF vent bacterial community. This microdiversity relates to the compositional fraction of aragonite, brucite, and calcite minerals within chimney samples rather than just the composition of nearby vent fluids. Although many species are found in both chimneys and venting fluids, the overall microbial community structures in chimney biofilms remain distinct from the hydrothermal fluids that flow through them. Shotgun metagenomic analyses reveal differences among genes predicted to be involved in carbon, methane, nitrogen and sulfur cycling with respect to their correlations to the abundances of specific minerals. These data hint at microenvironmental complexity lost within standard bulk analyses. The findings of this study underscore the need to more closely examine microbe-mineral interactions in natural environments, critically informing not just population-level distributions, but also the functional underpinnings of these extremophile microbial communities.https://www.frontiersin.org/articles/10.3389/frmbi.2024.1401831/fullhydrothermal ventgeomicrobiologycorrelationsmicrobe-rock interactionsextremophileLost City Hydrothermal Field
spellingShingle Osama M. Alian
William J. Brazelton
Karmina A. Aquino
Katrina I. Twing
H. Lizethe Pendleton
Gretchen Früh-Green
Susan Q. Lang
Matthew O. Schrenk
Matthew O. Schrenk
Microbial community differentiation in vent chimneys of the Lost City Hydrothermal Field reflects habitat heterogeneity
Frontiers in Microbiomes
hydrothermal vent
geomicrobiology
correlations
microbe-rock interactions
extremophile
Lost City Hydrothermal Field
title Microbial community differentiation in vent chimneys of the Lost City Hydrothermal Field reflects habitat heterogeneity
title_full Microbial community differentiation in vent chimneys of the Lost City Hydrothermal Field reflects habitat heterogeneity
title_fullStr Microbial community differentiation in vent chimneys of the Lost City Hydrothermal Field reflects habitat heterogeneity
title_full_unstemmed Microbial community differentiation in vent chimneys of the Lost City Hydrothermal Field reflects habitat heterogeneity
title_short Microbial community differentiation in vent chimneys of the Lost City Hydrothermal Field reflects habitat heterogeneity
title_sort microbial community differentiation in vent chimneys of the lost city hydrothermal field reflects habitat heterogeneity
topic hydrothermal vent
geomicrobiology
correlations
microbe-rock interactions
extremophile
Lost City Hydrothermal Field
url https://www.frontiersin.org/articles/10.3389/frmbi.2024.1401831/full
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