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Long-Term Incubation of Lake Water Enables Genomic Sampling of Consortia Involving Planctomycetes and Candidate Phyla Radiation Bacteria

Microbial communities in lakes can profoundly impact biogeochemical processes through their individual activities and collective interactions. However, the complexity of these communities poses challenges, particularly for studying rare organisms such as Candidate Phyla Radiation bacteria (CPR) and...

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Autores principales: Jaffe, Alexander L., Fuster, Maxime, Schoelmerich, Marie C., Chen, Lin-Xing, Colombet, Jonathan, Billard, Hermine, Sime-Ngando, Télesphore, Banfield, Jillian F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9040852/
https://www.ncbi.nlm.nih.gov/pubmed/35353011
http://dx.doi.org/10.1128/msystems.00223-22
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author Jaffe, Alexander L.
Fuster, Maxime
Schoelmerich, Marie C.
Chen, Lin-Xing
Colombet, Jonathan
Billard, Hermine
Sime-Ngando, Télesphore
Banfield, Jillian F.
author_facet Jaffe, Alexander L.
Fuster, Maxime
Schoelmerich, Marie C.
Chen, Lin-Xing
Colombet, Jonathan
Billard, Hermine
Sime-Ngando, Télesphore
Banfield, Jillian F.
author_sort Jaffe, Alexander L.
collection PubMed
description Microbial communities in lakes can profoundly impact biogeochemical processes through their individual activities and collective interactions. However, the complexity of these communities poses challenges, particularly for studying rare organisms such as Candidate Phyla Radiation bacteria (CPR) and enigmatic entities such as aster-like nanoparticles (ALNs). Here, a reactor was inoculated with water from Lake Fargette, France, and maintained under dark conditions at 4°C for 31 months and enriched for ALNs, diverse Planctomycetes, and CPR bacteria. We reconstructed draft genomes and predicted metabolic traits for 12 diverse Planctomycetes and 9 CPR bacteria, some of which are likely representatives of undescribed families or genera. One CPR genome representing the little-studied lineage “Candidatus Peribacter” was curated to completion (1.239 Mbp) and unexpectedly encodes the full gluconeogenesis pathway. Metatranscriptomic data indicate that some planctomycetes and CPR bacteria were active under the culture conditions, accounting for ∼30% and ∼1% of RNA reads mapping to the genome set, respectively. We also reconstructed genomes and obtained transmission electron microscope images for numerous viruses, including one with a >300-kbp genome and several predicted to infect Planctomycetes. Together, our analyses suggest that freshwater Planctomycetes are central players in a subsystem that includes ALNs, symbiotic CPR bacteria, and viruses. IMPORTANCE Laboratory incubations of natural microbial communities can aid in the study of member organisms and their networks of interaction. This is particularly important for understudied lineages for which key elements of basic biology are still emerging. Using genomics and microscopy, we found that members of the bacterial lineage Planctomycetes may be central players in a subset of a freshwater lake microbiome that includes other bacteria, archaea, viruses, and mysterious entities, called aster-like nanoparticles (ALNs), whose origin is unknown. Our results help constrain the possible origins of ALNs and provide insight into possible interactions within a complex lake ecosystem.
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spelling pubmed-90408522022-04-27 Long-Term Incubation of Lake Water Enables Genomic Sampling of Consortia Involving Planctomycetes and Candidate Phyla Radiation Bacteria Jaffe, Alexander L. Fuster, Maxime Schoelmerich, Marie C. Chen, Lin-Xing Colombet, Jonathan Billard, Hermine Sime-Ngando, Télesphore Banfield, Jillian F. mSystems Observation Microbial communities in lakes can profoundly impact biogeochemical processes through their individual activities and collective interactions. However, the complexity of these communities poses challenges, particularly for studying rare organisms such as Candidate Phyla Radiation bacteria (CPR) and enigmatic entities such as aster-like nanoparticles (ALNs). Here, a reactor was inoculated with water from Lake Fargette, France, and maintained under dark conditions at 4°C for 31 months and enriched for ALNs, diverse Planctomycetes, and CPR bacteria. We reconstructed draft genomes and predicted metabolic traits for 12 diverse Planctomycetes and 9 CPR bacteria, some of which are likely representatives of undescribed families or genera. One CPR genome representing the little-studied lineage “Candidatus Peribacter” was curated to completion (1.239 Mbp) and unexpectedly encodes the full gluconeogenesis pathway. Metatranscriptomic data indicate that some planctomycetes and CPR bacteria were active under the culture conditions, accounting for ∼30% and ∼1% of RNA reads mapping to the genome set, respectively. We also reconstructed genomes and obtained transmission electron microscope images for numerous viruses, including one with a >300-kbp genome and several predicted to infect Planctomycetes. Together, our analyses suggest that freshwater Planctomycetes are central players in a subsystem that includes ALNs, symbiotic CPR bacteria, and viruses. IMPORTANCE Laboratory incubations of natural microbial communities can aid in the study of member organisms and their networks of interaction. This is particularly important for understudied lineages for which key elements of basic biology are still emerging. Using genomics and microscopy, we found that members of the bacterial lineage Planctomycetes may be central players in a subset of a freshwater lake microbiome that includes other bacteria, archaea, viruses, and mysterious entities, called aster-like nanoparticles (ALNs), whose origin is unknown. Our results help constrain the possible origins of ALNs and provide insight into possible interactions within a complex lake ecosystem. American Society for Microbiology 2022-03-30 /pmc/articles/PMC9040852/ /pubmed/35353011 http://dx.doi.org/10.1128/msystems.00223-22 Text en Copyright © 2022 Jaffe et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Observation
Jaffe, Alexander L.
Fuster, Maxime
Schoelmerich, Marie C.
Chen, Lin-Xing
Colombet, Jonathan
Billard, Hermine
Sime-Ngando, Télesphore
Banfield, Jillian F.
Long-Term Incubation of Lake Water Enables Genomic Sampling of Consortia Involving Planctomycetes and Candidate Phyla Radiation Bacteria
title Long-Term Incubation of Lake Water Enables Genomic Sampling of Consortia Involving Planctomycetes and Candidate Phyla Radiation Bacteria
title_full Long-Term Incubation of Lake Water Enables Genomic Sampling of Consortia Involving Planctomycetes and Candidate Phyla Radiation Bacteria
title_fullStr Long-Term Incubation of Lake Water Enables Genomic Sampling of Consortia Involving Planctomycetes and Candidate Phyla Radiation Bacteria
title_full_unstemmed Long-Term Incubation of Lake Water Enables Genomic Sampling of Consortia Involving Planctomycetes and Candidate Phyla Radiation Bacteria
title_short Long-Term Incubation of Lake Water Enables Genomic Sampling of Consortia Involving Planctomycetes and Candidate Phyla Radiation Bacteria
title_sort long-term incubation of lake water enables genomic sampling of consortia involving planctomycetes and candidate phyla radiation bacteria
topic Observation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9040852/
https://www.ncbi.nlm.nih.gov/pubmed/35353011
http://dx.doi.org/10.1128/msystems.00223-22
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