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The economical lifestyle of CPR bacteria in groundwater allows little preference for environmental drivers

BACKGROUND: The highly diverse Cand. Patescibacteria are predicted to have minimal biosynthetic and metabolic pathways, which hinders understanding of how their populations differentiate in response to environmental drivers or host organisms. Their mechanisms employed to cope with oxidative stress a...

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Autores principales: Chaudhari, Narendrakumar M., Overholt, Will A., Figueroa-Gonzalez, Perla Abigail, Taubert, Martin, Bornemann, Till L. V., Probst, Alexander J., Hölzer, Martin, Marz, Manja, Küsel, Kirsten
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8672522/
https://www.ncbi.nlm.nih.gov/pubmed/34906246
http://dx.doi.org/10.1186/s40793-021-00395-w
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author Chaudhari, Narendrakumar M.
Overholt, Will A.
Figueroa-Gonzalez, Perla Abigail
Taubert, Martin
Bornemann, Till L. V.
Probst, Alexander J.
Hölzer, Martin
Marz, Manja
Küsel, Kirsten
author_facet Chaudhari, Narendrakumar M.
Overholt, Will A.
Figueroa-Gonzalez, Perla Abigail
Taubert, Martin
Bornemann, Till L. V.
Probst, Alexander J.
Hölzer, Martin
Marz, Manja
Küsel, Kirsten
author_sort Chaudhari, Narendrakumar M.
collection PubMed
description BACKGROUND: The highly diverse Cand. Patescibacteria are predicted to have minimal biosynthetic and metabolic pathways, which hinders understanding of how their populations differentiate in response to environmental drivers or host organisms. Their mechanisms employed to cope with oxidative stress are largely unknown. Here, we utilized genome-resolved metagenomics to investigate the adaptive genome repertoire of Patescibacteria in oxic and anoxic groundwaters, and to infer putative host ranges. RESULTS: Within six groundwater wells, Cand. Patescibacteria was the most dominant (up to 79%) super-phylum across 32 metagenomes sequenced from DNA retained on 0.2 and 0.1 µm filters after sequential filtration. Of the reconstructed 1275 metagenome-assembled genomes (MAGs), 291 high-quality MAGs were classified as Cand. Patescibacteria. Cand. Paceibacteria and Cand. Microgenomates were enriched exclusively in the 0.1 µm fractions, whereas candidate division ABY1 and Cand. Gracilibacteria were enriched in the 0.2 µm fractions. On average, Patescibacteria enriched in the smaller 0.1 µm filter fractions had 22% smaller genomes, 13.4% lower replication measures, higher proportion of rod-shape determining proteins, and of genomic features suggesting type IV pili mediated cell–cell attachments. Near-surface wells harbored Patescibacteria with higher replication rates than anoxic downstream wells characterized by longer water residence time. Except prevalence of superoxide dismutase genes in Patescibacteria MAGs enriched in oxic groundwaters (83%), no major metabolic or phylogenetic differences were observed. The most abundant Patescibacteria MAG in oxic groundwater encoded a nitrate transporter, nitrite reductase, and F-type ATPase, suggesting an alternative energy conservation mechanism. Patescibacteria consistently co-occurred with one another or with members of phyla Nanoarchaeota, Bacteroidota, Nitrospirota, and Omnitrophota. Among the MAGs enriched in 0.2 µm fractions,, only 8% Patescibacteria showed highly significant one-to-one correlation, mostly with Omnitrophota. Motility and transport related genes in certain Patescibacteria were highly similar to genes from other phyla (Omnitrophota, Proteobacteria and Nanoarchaeota). CONCLUSION: Other than genes to cope with oxidative stress, we found little genomic evidence for niche adaptation of Patescibacteria to oxic or anoxic groundwaters. Given that we could detect specific host preference only for a few MAGs, we speculate that the majority of Patescibacteria is able to attach multiple hosts just long enough to loot or exchange supplies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-021-00395-w.
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spelling pubmed-86725222021-12-16 The economical lifestyle of CPR bacteria in groundwater allows little preference for environmental drivers Chaudhari, Narendrakumar M. Overholt, Will A. Figueroa-Gonzalez, Perla Abigail Taubert, Martin Bornemann, Till L. V. Probst, Alexander J. Hölzer, Martin Marz, Manja Küsel, Kirsten Environ Microbiome Research Article BACKGROUND: The highly diverse Cand. Patescibacteria are predicted to have minimal biosynthetic and metabolic pathways, which hinders understanding of how their populations differentiate in response to environmental drivers or host organisms. Their mechanisms employed to cope with oxidative stress are largely unknown. Here, we utilized genome-resolved metagenomics to investigate the adaptive genome repertoire of Patescibacteria in oxic and anoxic groundwaters, and to infer putative host ranges. RESULTS: Within six groundwater wells, Cand. Patescibacteria was the most dominant (up to 79%) super-phylum across 32 metagenomes sequenced from DNA retained on 0.2 and 0.1 µm filters after sequential filtration. Of the reconstructed 1275 metagenome-assembled genomes (MAGs), 291 high-quality MAGs were classified as Cand. Patescibacteria. Cand. Paceibacteria and Cand. Microgenomates were enriched exclusively in the 0.1 µm fractions, whereas candidate division ABY1 and Cand. Gracilibacteria were enriched in the 0.2 µm fractions. On average, Patescibacteria enriched in the smaller 0.1 µm filter fractions had 22% smaller genomes, 13.4% lower replication measures, higher proportion of rod-shape determining proteins, and of genomic features suggesting type IV pili mediated cell–cell attachments. Near-surface wells harbored Patescibacteria with higher replication rates than anoxic downstream wells characterized by longer water residence time. Except prevalence of superoxide dismutase genes in Patescibacteria MAGs enriched in oxic groundwaters (83%), no major metabolic or phylogenetic differences were observed. The most abundant Patescibacteria MAG in oxic groundwater encoded a nitrate transporter, nitrite reductase, and F-type ATPase, suggesting an alternative energy conservation mechanism. Patescibacteria consistently co-occurred with one another or with members of phyla Nanoarchaeota, Bacteroidota, Nitrospirota, and Omnitrophota. Among the MAGs enriched in 0.2 µm fractions,, only 8% Patescibacteria showed highly significant one-to-one correlation, mostly with Omnitrophota. Motility and transport related genes in certain Patescibacteria were highly similar to genes from other phyla (Omnitrophota, Proteobacteria and Nanoarchaeota). CONCLUSION: Other than genes to cope with oxidative stress, we found little genomic evidence for niche adaptation of Patescibacteria to oxic or anoxic groundwaters. Given that we could detect specific host preference only for a few MAGs, we speculate that the majority of Patescibacteria is able to attach multiple hosts just long enough to loot or exchange supplies. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-021-00395-w. BioMed Central 2021-12-14 /pmc/articles/PMC8672522/ /pubmed/34906246 http://dx.doi.org/10.1186/s40793-021-00395-w Text en © The Author(s) 2021 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 Article
Chaudhari, Narendrakumar M.
Overholt, Will A.
Figueroa-Gonzalez, Perla Abigail
Taubert, Martin
Bornemann, Till L. V.
Probst, Alexander J.
Hölzer, Martin
Marz, Manja
Küsel, Kirsten
The economical lifestyle of CPR bacteria in groundwater allows little preference for environmental drivers
title The economical lifestyle of CPR bacteria in groundwater allows little preference for environmental drivers
title_full The economical lifestyle of CPR bacteria in groundwater allows little preference for environmental drivers
title_fullStr The economical lifestyle of CPR bacteria in groundwater allows little preference for environmental drivers
title_full_unstemmed The economical lifestyle of CPR bacteria in groundwater allows little preference for environmental drivers
title_short The economical lifestyle of CPR bacteria in groundwater allows little preference for environmental drivers
title_sort economical lifestyle of cpr bacteria in groundwater allows little preference for environmental drivers
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8672522/
https://www.ncbi.nlm.nih.gov/pubmed/34906246
http://dx.doi.org/10.1186/s40793-021-00395-w
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