Cargando…

Spatially resolved correlative microscopy and microbial identification reveal dynamic depth‐ and mineral‐dependent anabolic activity in salt marsh sediment

Coastal salt marshes are key sites of biogeochemical cycling and ideal systems in which to investigate the community structure of complex microbial communities. Here, we clarify structural–functional relationships among microorganisms and their mineralogical environment, revealing previously undescr...

Descripción completa

Detalles Bibliográficos
Autores principales: Marlow, Jeffrey, Spietz, Rachel, Kim, Keun‐Young, Ellisman, Mark, Girguis, Peter, Hatzenpichler, Roland
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8456820/
https://www.ncbi.nlm.nih.gov/pubmed/34346142
http://dx.doi.org/10.1111/1462-2920.15667
_version_ 1784570946558885888
author Marlow, Jeffrey
Spietz, Rachel
Kim, Keun‐Young
Ellisman, Mark
Girguis, Peter
Hatzenpichler, Roland
author_facet Marlow, Jeffrey
Spietz, Rachel
Kim, Keun‐Young
Ellisman, Mark
Girguis, Peter
Hatzenpichler, Roland
author_sort Marlow, Jeffrey
collection PubMed
description Coastal salt marshes are key sites of biogeochemical cycling and ideal systems in which to investigate the community structure of complex microbial communities. Here, we clarify structural–functional relationships among microorganisms and their mineralogical environment, revealing previously undescribed metabolic activity patterns and precise spatial arrangements within salt marsh sediment. Following 3.7‐day in situ incubations with a non‐canonical amino acid that was incorporated into new biomass, samples were resin‐embedded and analysed by correlative fluorescence and electron microscopy to map the microscale arrangements of anabolically active and inactive organisms alongside mineral grains. Parallel sediment samples were examined by fluorescence‐activated cell sorting and 16S rRNA gene sequencing to link anabolic activity to taxonomic identity. Both approaches demonstrated a rapid decline in the proportion of anabolically active cells with depth into salt marsh sediment, from ~60% in the top centimetre to 9.4%–22.4% between 2 and 10 cm. From the top to the bottom, the most prominent active community members shifted from sulfur cycling phototrophic consortia, to putative sulfate‐reducing bacteria likely oxidizing organic compounds, to fermentative lineages. Correlative microscopy revealed more abundant (and more anabolically active) organisms around non‐quartz minerals including rutile, orthoclase and plagioclase. Microbe–mineral relationships appear to be dynamic and context‐dependent arbiters of biogeochemical cycling.
format Online
Article
Text
id pubmed-8456820
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher John Wiley & Sons, Inc.
record_format MEDLINE/PubMed
spelling pubmed-84568202021-09-27 Spatially resolved correlative microscopy and microbial identification reveal dynamic depth‐ and mineral‐dependent anabolic activity in salt marsh sediment Marlow, Jeffrey Spietz, Rachel Kim, Keun‐Young Ellisman, Mark Girguis, Peter Hatzenpichler, Roland Environ Microbiol Research Articles Coastal salt marshes are key sites of biogeochemical cycling and ideal systems in which to investigate the community structure of complex microbial communities. Here, we clarify structural–functional relationships among microorganisms and their mineralogical environment, revealing previously undescribed metabolic activity patterns and precise spatial arrangements within salt marsh sediment. Following 3.7‐day in situ incubations with a non‐canonical amino acid that was incorporated into new biomass, samples were resin‐embedded and analysed by correlative fluorescence and electron microscopy to map the microscale arrangements of anabolically active and inactive organisms alongside mineral grains. Parallel sediment samples were examined by fluorescence‐activated cell sorting and 16S rRNA gene sequencing to link anabolic activity to taxonomic identity. Both approaches demonstrated a rapid decline in the proportion of anabolically active cells with depth into salt marsh sediment, from ~60% in the top centimetre to 9.4%–22.4% between 2 and 10 cm. From the top to the bottom, the most prominent active community members shifted from sulfur cycling phototrophic consortia, to putative sulfate‐reducing bacteria likely oxidizing organic compounds, to fermentative lineages. Correlative microscopy revealed more abundant (and more anabolically active) organisms around non‐quartz minerals including rutile, orthoclase and plagioclase. Microbe–mineral relationships appear to be dynamic and context‐dependent arbiters of biogeochemical cycling. John Wiley & Sons, Inc. 2021-08-04 2021-08 /pmc/articles/PMC8456820/ /pubmed/34346142 http://dx.doi.org/10.1111/1462-2920.15667 Text en © 2021 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Research Articles
Marlow, Jeffrey
Spietz, Rachel
Kim, Keun‐Young
Ellisman, Mark
Girguis, Peter
Hatzenpichler, Roland
Spatially resolved correlative microscopy and microbial identification reveal dynamic depth‐ and mineral‐dependent anabolic activity in salt marsh sediment
title Spatially resolved correlative microscopy and microbial identification reveal dynamic depth‐ and mineral‐dependent anabolic activity in salt marsh sediment
title_full Spatially resolved correlative microscopy and microbial identification reveal dynamic depth‐ and mineral‐dependent anabolic activity in salt marsh sediment
title_fullStr Spatially resolved correlative microscopy and microbial identification reveal dynamic depth‐ and mineral‐dependent anabolic activity in salt marsh sediment
title_full_unstemmed Spatially resolved correlative microscopy and microbial identification reveal dynamic depth‐ and mineral‐dependent anabolic activity in salt marsh sediment
title_short Spatially resolved correlative microscopy and microbial identification reveal dynamic depth‐ and mineral‐dependent anabolic activity in salt marsh sediment
title_sort spatially resolved correlative microscopy and microbial identification reveal dynamic depth‐ and mineral‐dependent anabolic activity in salt marsh sediment
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8456820/
https://www.ncbi.nlm.nih.gov/pubmed/34346142
http://dx.doi.org/10.1111/1462-2920.15667
work_keys_str_mv AT marlowjeffrey spatiallyresolvedcorrelativemicroscopyandmicrobialidentificationrevealdynamicdepthandmineraldependentanabolicactivityinsaltmarshsediment
AT spietzrachel spatiallyresolvedcorrelativemicroscopyandmicrobialidentificationrevealdynamicdepthandmineraldependentanabolicactivityinsaltmarshsediment
AT kimkeunyoung spatiallyresolvedcorrelativemicroscopyandmicrobialidentificationrevealdynamicdepthandmineraldependentanabolicactivityinsaltmarshsediment
AT ellismanmark spatiallyresolvedcorrelativemicroscopyandmicrobialidentificationrevealdynamicdepthandmineraldependentanabolicactivityinsaltmarshsediment
AT girguispeter spatiallyresolvedcorrelativemicroscopyandmicrobialidentificationrevealdynamicdepthandmineraldependentanabolicactivityinsaltmarshsediment
AT hatzenpichlerroland spatiallyresolvedcorrelativemicroscopyandmicrobialidentificationrevealdynamicdepthandmineraldependentanabolicactivityinsaltmarshsediment