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

Cand. Patescibacteria Candidate phyla radiation (CPR) Economic lifestyle Metagenomics Microbial ecology

Journal

Environmental microbiome
ISSN: 2524-6372
Titre abrégé: Environ Microbiome
Pays: England
ID NLM: 101768168

Informations de publication

Date de publication:
14 Dec 2021
Historique:
received: 20 10 2021
accepted: 03 12 2021
entrez: 15 12 2021
pubmed: 16 12 2021
medline: 16 12 2021
Statut: epublish

Résumé

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. 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). 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.

Sections du résumé

BACKGROUND 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 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 CONCLUSIONS
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.

Identifiants

pubmed: 34906246
doi: 10.1186/s40793-021-00395-w
pii: 10.1186/s40793-021-00395-w
pmc: PMC8672522
doi:

Types de publication

Journal Article

Langues

eng

Pagination

24

Subventions

Organisme : deutsche forschungsgemeinschaft
ID : SFB 1076 -Project Number 218627073
Organisme : deutsche forschungsgemeinschaft
ID : FZT 118 - 202548816
Organisme : deutsche forschungsgemeinschaft
ID : Germany's Excellence Strategy - EXC 2051 - Project-ID 390713860
Organisme : ministerium für kultur und wissenschaft des landes nordrhein-westfalen
ID : Nachwuchsgruppe Dr. Alexander Probst

Informations de copyright

© 2021. The Author(s).

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Auteurs

Narendrakumar M Chaudhari (NM)

Aquatic Geomicrobiology, Institute of Biodiversity, Friedrich Schiller University, Jena, Germany.
German Center for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany.

Will A Overholt (WA)

Aquatic Geomicrobiology, Institute of Biodiversity, Friedrich Schiller University, Jena, Germany.

Perla Abigail Figueroa-Gonzalez (PA)

Department for Chemistry, Environmental Microbiology and Biotechnology, Group for Aquatic Microbial Ecology (GAME), University Duisburg-Essen, Essen, Germany.

Martin Taubert (M)

Aquatic Geomicrobiology, Institute of Biodiversity, Friedrich Schiller University, Jena, Germany.

Till L V Bornemann (TLV)

Department for Chemistry, Environmental Microbiology and Biotechnology, Group for Aquatic Microbial Ecology (GAME), University Duisburg-Essen, Essen, Germany.

Alexander J Probst (AJ)

Department for Chemistry, Environmental Microbiology and Biotechnology, Group for Aquatic Microbial Ecology (GAME), University Duisburg-Essen, Essen, Germany.

Martin Hölzer (M)

RNA Bioinformatics and High Throughput Analysis, Friedrich Schiller University, Jena, Germany.
European Virus Bioinformatics Center, Friedrich Schiller University, Jena, Germany.
Methodology and Research Infrastructure, MF1 Bioinformatics, Robert Koch Institute, Berlin, Germany.

Manja Marz (M)

RNA Bioinformatics and High Throughput Analysis, Friedrich Schiller University, Jena, Germany.
European Virus Bioinformatics Center, Friedrich Schiller University, Jena, Germany.
FLI Leibniz Institute for Age Research, Jena, Germany.

Kirsten Küsel (K)

Aquatic Geomicrobiology, Institute of Biodiversity, Friedrich Schiller University, Jena, Germany. kirsten.kuesel@uni-jena.de.
German Center for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany. kirsten.kuesel@uni-jena.de.

Classifications MeSH