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Environmental Microbiology | Spotlight

Evidence for a Growth Zone for Deep-Subsurface Microbial Clades in Near-Surface Anoxic Sediments

Karen G. Lloyd, Jordan T. Bird, Joy Buongiorno, Emily Deas, Richard Kevorkian, Talor Noordhoek, Jacob Rosalsky, Taylor Roy
Alfons J. M. Stams, Editor
Karen G. Lloyd
aUniversity of Tennessee, Knoxville, Tennessee, USA
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Jordan T. Bird
aUniversity of Tennessee, Knoxville, Tennessee, USA
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Joy Buongiorno
aUniversity of Tennessee, Knoxville, Tennessee, USA
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Emily Deas
aUniversity of Tennessee, Knoxville, Tennessee, USA
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Richard Kevorkian
aUniversity of Tennessee, Knoxville, Tennessee, USA
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Talor Noordhoek
aUniversity of Tennessee, Knoxville, Tennessee, USA
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Jacob Rosalsky
aUniversity of Tennessee, Knoxville, Tennessee, USA
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Taylor Roy
aUniversity of Tennessee, Knoxville, Tennessee, USA
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Alfons J. M. Stams
Wageningen University
Roles: Editor
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DOI: 10.1128/AEM.00877-20
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This article has a correction. Please see:

  • Erratum for Lloyd et al., “Evidence for a Growth Zone for Deep-Subsurface Microbial Clades in Near-Surface Anoxic Sediments” - October 15, 2020

ABSTRACT

Global marine sediments harbor a large and highly diverse microbial biosphere, but the mechanism by which this biosphere is established during sediment burial is largely unknown. During burial in marine sediments, concentrations of easily metabolized organic compounds and total microbial cell abundance decrease. However, it is unknown whether some microbial clades increase with depth. We show total population increases in 38 microbial families over 3 cm of sediment depth in the upper 7.5 cm of White Oak River (WOR) estuary sediments. Clades that increased with depth were more often associated with one or more of the following: anaerobes, uncultured, or common in deep marine sediments relative to those that decreased. Maximum doubling times (in situ steady-state growth rates could be faster to balance cell decay) were estimated as 2 to 25 years by combining sedimentation rate with either quantitative PCR (qPCR) or the product of the fraction read abundance of 16S rRNA genes and total cell counts (FRAxC). Doubling times were within an order of magnitude of each other in two adjacent cores, as well as in two laboratory enrichments of Cape Lookout Bight (CLB), NC, sediments (average difference of 28% ± 19%). qPCR and FRAxC in sediment cores and laboratory enrichments produced similar doubling times for key deep subsurface uncultured clades Bathyarchaeota (8.7 ± 1.9 years) and Thermoprofundales/MBG-D (4.1 ± 0.7 years). We conclude that common deep subsurface microbial clades experience a narrow zone of growth in shallow sediments, offering an opportunity for selection of long-term subsistence traits after resuspension events.

IMPORTANCE Many studies show that the uncultured microbes that dominate global marine sediments do not actually increase in population size as they are buried in marine sediments; rather, they exist in a sort of prolonged torpor for thousands of years. This is because, although studies have shown biomass turnover in these clades, no evidence has ever been found that deeper sediments have larger populations for specific clades than shallower layers. We discovered that they actually do increase population sizes during burial, but only in the upper few centimeters. This suggests that marine sediments may be a vast repository of mostly nongrowing microbes with a thin and relatively rapid area of cell abundance increase in the upper 10 cm, offering a chance for subsurface organisms to undergo natural selection.

FOOTNOTES

    • Received 11 April 2020.
    • Accepted 17 July 2020.
    • Accepted manuscript posted online 24 July 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

All Rights Reserved.

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Evidence for a Growth Zone for Deep-Subsurface Microbial Clades in Near-Surface Anoxic Sediments
Karen G. Lloyd, Jordan T. Bird, Joy Buongiorno, Emily Deas, Richard Kevorkian, Talor Noordhoek, Jacob Rosalsky, Taylor Roy
Applied and Environmental Microbiology Sep 2020, 86 (19) e00877-20; DOI: 10.1128/AEM.00877-20

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Evidence for a Growth Zone for Deep-Subsurface Microbial Clades in Near-Surface Anoxic Sediments
Karen G. Lloyd, Jordan T. Bird, Joy Buongiorno, Emily Deas, Richard Kevorkian, Talor Noordhoek, Jacob Rosalsky, Taylor Roy
Applied and Environmental Microbiology Sep 2020, 86 (19) e00877-20; DOI: 10.1128/AEM.00877-20
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KEYWORDS

biogeochemistry
marine sediments
subsurface biosphere

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