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Variable impact of geochemical gradients on the functional potential of bacteria, archaea, and phages from the permanently stratified Lac Pavin

BACKGROUND: Permanently stratified lakes contain diverse microbial communities that vary with depth and so serve as useful models for studying the relationships between microbial community structure and geochemistry. Recent work has shown that these lakes can also harbor numerous bacteria and archae...

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Autores principales: Jaffe, Alexander L., Bardot, Corinne, Le Jeune, Anne-Hélène, Liu, Jett, Colombet, Jonathan, Perrière, Fanny, Billard, Hermine, Castelle, Cindy J., Lehours, Anne-Catherine, Banfield, Jillian F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9875498/
https://www.ncbi.nlm.nih.gov/pubmed/36694212
http://dx.doi.org/10.1186/s40168-022-01416-7
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author Jaffe, Alexander L.
Bardot, Corinne
Le Jeune, Anne-Hélène
Liu, Jett
Colombet, Jonathan
Perrière, Fanny
Billard, Hermine
Castelle, Cindy J.
Lehours, Anne-Catherine
Banfield, Jillian F.
author_facet Jaffe, Alexander L.
Bardot, Corinne
Le Jeune, Anne-Hélène
Liu, Jett
Colombet, Jonathan
Perrière, Fanny
Billard, Hermine
Castelle, Cindy J.
Lehours, Anne-Catherine
Banfield, Jillian F.
author_sort Jaffe, Alexander L.
collection PubMed
description BACKGROUND: Permanently stratified lakes contain diverse microbial communities that vary with depth and so serve as useful models for studying the relationships between microbial community structure and geochemistry. Recent work has shown that these lakes can also harbor numerous bacteria and archaea from novel lineages, including those from the Candidate Phyla Radiation (CPR). However, the extent to which geochemical stratification differentially impacts carbon metabolism and overall genetic potential in CPR bacteria compared to other organisms is not well defined. RESULTS: Here, we determine the distribution of microbial lineages along an oxygen gradient in Lac Pavin, a deep, stratified lake in central France, and examine the influence of this gradient on their metabolism. Genome-based analyses revealed an enrichment of distinct C1 and CO(2) fixation pathways in the oxic lake interface and anoxic zone/sediments, suggesting that oxygen likely plays a role in structuring metabolic strategies in non-CPR bacteria and archaea. Notably, we find that the oxidation of methane and its byproducts is largely spatially separated from methane production, which is mediated by diverse communities of sediment methanogens that vary on the centimeter scale. In contrast, we detected evidence for RuBisCO throughout the water column and sediments, including form II/III and form III-related enzymes encoded by CPR bacteria in the water column and DPANN archaea in the sediments. On the whole, though, CPR bacteria and phages did not show strong signals of gene content differentiation by depth, despite the fact that distinct species groups populate different lake and sediment compartments. CONCLUSIONS: Overall, our analyses suggest that environmental gradients in Lac Pavin select for capacities of CPR bacteria and phages to a lesser extent than for other bacteria and archaea. This may be due to the fact that selection in the former groups is indirect and depends primarily on host characteristics. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01416-7.
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spelling pubmed-98754982023-01-26 Variable impact of geochemical gradients on the functional potential of bacteria, archaea, and phages from the permanently stratified Lac Pavin Jaffe, Alexander L. Bardot, Corinne Le Jeune, Anne-Hélène Liu, Jett Colombet, Jonathan Perrière, Fanny Billard, Hermine Castelle, Cindy J. Lehours, Anne-Catherine Banfield, Jillian F. Microbiome Research BACKGROUND: Permanently stratified lakes contain diverse microbial communities that vary with depth and so serve as useful models for studying the relationships between microbial community structure and geochemistry. Recent work has shown that these lakes can also harbor numerous bacteria and archaea from novel lineages, including those from the Candidate Phyla Radiation (CPR). However, the extent to which geochemical stratification differentially impacts carbon metabolism and overall genetic potential in CPR bacteria compared to other organisms is not well defined. RESULTS: Here, we determine the distribution of microbial lineages along an oxygen gradient in Lac Pavin, a deep, stratified lake in central France, and examine the influence of this gradient on their metabolism. Genome-based analyses revealed an enrichment of distinct C1 and CO(2) fixation pathways in the oxic lake interface and anoxic zone/sediments, suggesting that oxygen likely plays a role in structuring metabolic strategies in non-CPR bacteria and archaea. Notably, we find that the oxidation of methane and its byproducts is largely spatially separated from methane production, which is mediated by diverse communities of sediment methanogens that vary on the centimeter scale. In contrast, we detected evidence for RuBisCO throughout the water column and sediments, including form II/III and form III-related enzymes encoded by CPR bacteria in the water column and DPANN archaea in the sediments. On the whole, though, CPR bacteria and phages did not show strong signals of gene content differentiation by depth, despite the fact that distinct species groups populate different lake and sediment compartments. CONCLUSIONS: Overall, our analyses suggest that environmental gradients in Lac Pavin select for capacities of CPR bacteria and phages to a lesser extent than for other bacteria and archaea. This may be due to the fact that selection in the former groups is indirect and depends primarily on host characteristics. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01416-7. BioMed Central 2023-01-25 /pmc/articles/PMC9875498/ /pubmed/36694212 http://dx.doi.org/10.1186/s40168-022-01416-7 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Jaffe, Alexander L.
Bardot, Corinne
Le Jeune, Anne-Hélène
Liu, Jett
Colombet, Jonathan
Perrière, Fanny
Billard, Hermine
Castelle, Cindy J.
Lehours, Anne-Catherine
Banfield, Jillian F.
Variable impact of geochemical gradients on the functional potential of bacteria, archaea, and phages from the permanently stratified Lac Pavin
title Variable impact of geochemical gradients on the functional potential of bacteria, archaea, and phages from the permanently stratified Lac Pavin
title_full Variable impact of geochemical gradients on the functional potential of bacteria, archaea, and phages from the permanently stratified Lac Pavin
title_fullStr Variable impact of geochemical gradients on the functional potential of bacteria, archaea, and phages from the permanently stratified Lac Pavin
title_full_unstemmed Variable impact of geochemical gradients on the functional potential of bacteria, archaea, and phages from the permanently stratified Lac Pavin
title_short Variable impact of geochemical gradients on the functional potential of bacteria, archaea, and phages from the permanently stratified Lac Pavin
title_sort variable impact of geochemical gradients on the functional potential of bacteria, archaea, and phages from the permanently stratified lac pavin
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9875498/
https://www.ncbi.nlm.nih.gov/pubmed/36694212
http://dx.doi.org/10.1186/s40168-022-01416-7
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