Microbial Diversity and Function in Shallow Subsurface Sediment and Oceanic Lithosphere of the Atlantis Massif

ABSTRACT The marine lithospheric subsurface is one of the largest biospheres on Earth; however, little is known about the identity and ecological function of microorganisms found in low abundance in this habitat, though these organisms impact global-scale biogeochemical cycling. Here, we describe th...

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Autores principales: J. Goordial, T. D’Angelo, J. M. Labonté, N. J. Poulton, J. M. Brown, R. Stepanauskas, G. L. Früh-Green, B. N. Orcutt
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Publicado: American Society for Microbiology 2021
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spelling oai:doaj.org-article:c90365e888394afa9d358cc0b4484db92021-11-10T18:37:50ZMicrobial Diversity and Function in Shallow Subsurface Sediment and Oceanic Lithosphere of the Atlantis Massif10.1128/mBio.00490-212150-7511https://doaj.org/article/c90365e888394afa9d358cc0b4484db92021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00490-21https://doaj.org/toc/2150-7511ABSTRACT The marine lithospheric subsurface is one of the largest biospheres on Earth; however, little is known about the identity and ecological function of microorganisms found in low abundance in this habitat, though these organisms impact global-scale biogeochemical cycling. Here, we describe the diversity and metabolic potential of sediment and endolithic (within rock) microbial communities found in ultrasmall amounts (101 to 104 cells cm−3) in the subsurface of the Atlantis Massif, an oceanic core complex on the Mid-Atlantic Ridge that was sampled on International Ocean Discovery Program (IODP) Expedition 357. This study used fluorescence-activated cell sorting (FACS) to enable the first amplicon, metagenomic, and single-cell genomic study of the shallow (<20 m below seafloor) subsurface of an actively serpentinizing marine system. The shallow subsurface biosphere of the Atlantis Massif was found to be distinct from communities observed in the nearby Lost City alkaline hydrothermal fluids and chimneys, yet similar to other low-temperature, aerobic subsurface settings. Genes associated with autotrophy were rare, although heterotrophy and aerobic carbon monoxide and formate cycling metabolisms were identified. Overall, this study reveals that the shallow subsurface of an oceanic core complex hosts a biosphere that is not fueled by active serpentinization reactions and by-products. IMPORTANCE The subsurface rock beneath the ocean is one of the largest biospheres on Earth, and microorganisms within influence global-scale nutrient cycles. This biosphere is difficult to study, in part due to the low concentrations of microorganisms that inhabit the vast volume of the marine lithosphere. In spite of the global significance of this biosphere, little is currently known about the microbial ecology of such rock-associated microorganisms. This study describes the identity and genomic potential of microorganisms in the subsurface rock and sediment at the Atlantis Massif, an underwater mountain near the Mid-Atlantic Ridge. To enable our analyses, fluorescence-activated cell sorting (FACS) was used as a means to concentrate cells from low biomass environmental samples for genomic analyses. We found distinct rock-associated microorganisms and found that the capacity for microorganisms to utilize organic carbon was the most prevalent form of carbon cycling. We additionally identified a potential role for carbon monoxide metabolism in the subsurface.J. GoordialT. D’AngeloJ. M. LabontéN. J. PoultonJ. M. BrownR. StepanauskasG. L. Früh-GreenB. N. OrcuttAmerican Society for MicrobiologyarticleAtlantis Massifdeep biosphereoceanic crustIODPsingle-cell genomicsfluorescence-activated cell sortingMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution DOAJ
collection DOAJ
language EN
topic Atlantis Massif
deep biosphere
oceanic crust
IODP
single-cell genomics
fluorescence-activated cell sorting
Microbiology
QR1-502
spellingShingle Atlantis Massif
deep biosphere
oceanic crust
IODP
single-cell genomics
fluorescence-activated cell sorting
Microbiology
QR1-502
J. Goordial
T. D’Angelo
J. M. Labonté
N. J. Poulton
J. M. Brown
R. Stepanauskas
G. L. Früh-Green
B. N. Orcutt
Microbial Diversity and Function in Shallow Subsurface Sediment and Oceanic Lithosphere of the Atlantis Massif
description ABSTRACT The marine lithospheric subsurface is one of the largest biospheres on Earth; however, little is known about the identity and ecological function of microorganisms found in low abundance in this habitat, though these organisms impact global-scale biogeochemical cycling. Here, we describe the diversity and metabolic potential of sediment and endolithic (within rock) microbial communities found in ultrasmall amounts (101 to 104 cells cm−3) in the subsurface of the Atlantis Massif, an oceanic core complex on the Mid-Atlantic Ridge that was sampled on International Ocean Discovery Program (IODP) Expedition 357. This study used fluorescence-activated cell sorting (FACS) to enable the first amplicon, metagenomic, and single-cell genomic study of the shallow (<20 m below seafloor) subsurface of an actively serpentinizing marine system. The shallow subsurface biosphere of the Atlantis Massif was found to be distinct from communities observed in the nearby Lost City alkaline hydrothermal fluids and chimneys, yet similar to other low-temperature, aerobic subsurface settings. Genes associated with autotrophy were rare, although heterotrophy and aerobic carbon monoxide and formate cycling metabolisms were identified. Overall, this study reveals that the shallow subsurface of an oceanic core complex hosts a biosphere that is not fueled by active serpentinization reactions and by-products. IMPORTANCE The subsurface rock beneath the ocean is one of the largest biospheres on Earth, and microorganisms within influence global-scale nutrient cycles. This biosphere is difficult to study, in part due to the low concentrations of microorganisms that inhabit the vast volume of the marine lithosphere. In spite of the global significance of this biosphere, little is currently known about the microbial ecology of such rock-associated microorganisms. This study describes the identity and genomic potential of microorganisms in the subsurface rock and sediment at the Atlantis Massif, an underwater mountain near the Mid-Atlantic Ridge. To enable our analyses, fluorescence-activated cell sorting (FACS) was used as a means to concentrate cells from low biomass environmental samples for genomic analyses. We found distinct rock-associated microorganisms and found that the capacity for microorganisms to utilize organic carbon was the most prevalent form of carbon cycling. We additionally identified a potential role for carbon monoxide metabolism in the subsurface.
format article
author J. Goordial
T. D’Angelo
J. M. Labonté
N. J. Poulton
J. M. Brown
R. Stepanauskas
G. L. Früh-Green
B. N. Orcutt
author_facet J. Goordial
T. D’Angelo
J. M. Labonté
N. J. Poulton
J. M. Brown
R. Stepanauskas
G. L. Früh-Green
B. N. Orcutt
author_sort J. Goordial
title Microbial Diversity and Function in Shallow Subsurface Sediment and Oceanic Lithosphere of the Atlantis Massif
title_short Microbial Diversity and Function in Shallow Subsurface Sediment and Oceanic Lithosphere of the Atlantis Massif
title_full Microbial Diversity and Function in Shallow Subsurface Sediment and Oceanic Lithosphere of the Atlantis Massif
title_fullStr Microbial Diversity and Function in Shallow Subsurface Sediment and Oceanic Lithosphere of the Atlantis Massif
title_full_unstemmed Microbial Diversity and Function in Shallow Subsurface Sediment and Oceanic Lithosphere of the Atlantis Massif
title_sort microbial diversity and function in shallow subsurface sediment and oceanic lithosphere of the atlantis massif
publisher American Society for Microbiology
publishDate 2021
url https://doaj.org/article/c90365e888394afa9d358cc0b4484db9
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