Dataset Information

Metabolic cooperation and spatiotemporal niche partitioning in a kefir microbial community.

ABSTRACT: Microbial communities often undergo intricate compositional changes yet also maintain stable coexistence of diverse species. The mechanisms underlying long-term coexistence remain unclear as system-wide studies have been largely limited to engineered communities, ex situ adapted cultures or synthetic assemblies. Here, we show how kefir, a natural milk-fermenting community of prokaryotes (predominantly lactic and acetic acid bacteria) and yeasts (family Saccharomycetaceae), realizes stable coexistence through spatiotemporal orchestration of species and metabolite dynamics. During milk fermentation, kefir grains (a polysaccharide matrix synthesized by kefir microorganisms) grow in mass but remain unchanged in composition. In contrast, the milk is colonized in a sequential manner in which early members open the niche for the followers by making available metabolites such as amino acids and lactate. Through metabolomics, transcriptomics and large-scale mapping of inter-species interactions, we show how microorganisms poorly suited for milk survive in-and even dominate-the community, through metabolic cooperation and uneven partitioning between grain and milk. Overall, our findings reveal how inter-species interactions partitioned in space and time lead to stable coexistence.

SUBMITTER: Blasche S

PROVIDER: S-EPMC7610452 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Metabolic cooperation and spatiotemporal niche partitioning in a kefir microbial community.

Blasche Sonja S Kim Yongkyu Y Kim Yongkyu Y Mars Ruben A T RAT Machado Daniel D Maansson Maria M Kafkia Eleni E Milanese Alessio A Zeller Georg G Teusink Bas B Nielsen Jens J Benes Vladimir V Neves Rute R Sauer Uwe U Patil Kiran Raosaheb KR

Nature microbiology 20210104 2

Microbial communities often undergo intricate compositional changes yet also maintain stable coexistence of diverse species. The mechanisms underlying long-term coexistence remain unclear as system-wide studies have been largely limited to engineered communities, ex situ adapted cultures or synthetic assemblies. Here, we show how kefir, a natural milk-fermenting community of prokaryotes (predominantly lactic and acetic acid bacteria) and yeasts (family Saccharomycetaceae), realizes stable coexis ...[more]

PMID: 33398099

Similar Datasets

Project description:Microbial communities often undergo intricate compositional changes yet also maintain stable coexistence of diverse species. The mechanisms underlying long-term coexistence remain unclear, as system-wide studies have been largely limited to engineered communities, ex situ adapted cultures, or synthetic assemblies. Here we show how kefir, a natural milk-fermenting community of prokaryotes and yeasts, realises stable coexistence through spatiotemporal orchestration of species and metabolite dynamics. During milk fermentation, kefir grains (a polysaccharide matrix synthesized by kefir microbes) grow in mass but remain unchanged in composition. In contrast, the milk is colonized in a sequential manner in which early members open metabolic niches for followers. Through metabolomics and large-scale mapping of inter-species interactions, we show how microbes poorly suited for milk survive in, and even dominate the community, through metabolic cooperation and uneven partitioning between grain and milk. Overall, our findings reveal how inter-species interactions partitioned in space and time lead to stable coexistence. Linked metabolomics studies:<a href='https://www.ebi.ac.uk/metabolights/MTBLS1823' rel='noopener noreferrer' target='_blank'>MTBLS1823</a> Spent-medium assay, measured untargeted (FIA-qTOF) and targeted (HILIC, LC-MS)<a href='https://www.ebi.ac.uk/metabolights/MTBLS1830' rel='noopener noreferrer' target='_blank'>MTBLS1830</a> Interaction between the kefir isolates Lactococcus lactis and Acetobacter fabarum (GC-MS) Linked cross omic data sets:Genomes of isolated kefir species are available in the NCBI database under the accession: PRJNA375758 (bioproject ID: 375758).Metatranscriptomic sequencing data associated with this study are available in the European Nucleotide Archive (ENA): accession number <a href='https://www.ebi.ac.uk/ena/browser/view/PRJEB37001' rel='noopener noreferrer' target='_blank'>PRJEB37001</a>.Genome-scale metabolic models for kefir bacteria can be found at github.com/cdanielmachado/kefir_models.

Project description:Microbial communities often undergo intricate compositional changes yet also maintain stable coexistence of diverse species. The mechanisms underlying long-term coexistence remain unclear, as system-wide studies have been largely limited to engineered communities, ex situ adapted cultures, or synthetic assemblies. Here we show how kefir, a natural milk-fermenting community of prokaryotes and yeasts, realizes stable coexistence through spatiotemporal orchestration of species and metabolite dynamics. During milk fermentation, kefir grains (a polysaccharide matrix synthesized by kefir microbes) grow in mass but remain unchanged in composition. In contrast, the milk is colonized in a sequential manner in which early members open metabolic niches for followers. Through metabolomics and large-scale mapping of inter-species interactions, we show how microbes poorly suited for milk survive in — and even dominate — the community, through metabolic cooperation and uneven partitioning between grain and milk. Overall, our findings reveal how inter-species interactions partitioned in space and time lead to stable coexistence. Linked metabolomics studies:<a href='https://www.ebi.ac.uk/metabolights/MTBLS1823' rel='noopener noreferrer' target='_blank'>MTBLS1823</a> Spent-medium assay, measured untargeted (FIA-qTOF) and targeted (HILIC, LC-MS)<a href='https://www.ebi.ac.uk/metabolights/MTBLS1829' rel='noopener noreferrer' target='_blank'>MTBLS1829</a> Kefir fermentation curve (FIA-MS) Linked cross omic data:Genomes of isolated kefir species are available in the <a href='https://www.ncbi.nlm.nih.gov/' rel='noopener noreferrer' target='_blank'>NCBI database</a> under the accession: PRJNA375758 (bioproject ID: 375758).Metatranscriptomic sequencing reads can be accessed from <a href='https://www.ebi.ac.uk/metabolights/editor/www.ebi.ac.uk/ena' rel='noopener noreferrer' target='_blank'>ENA</a> under the project id PRJEB37001.Genome-scale metabolic models for kefir bacteria can be found at github.com/cdanielmachado/kefir_models.

Project description:Microbial communities often undergo intricate compositional changes yet also maintain stable coexistence of diverse species. The mechanisms underlying long-term coexistence remain unclear, as system-wide studies have been largely limited to engineered communities, ex situ adapted cultures, or synthetic assemblies. Here we show how kefir, a natural milk-fermenting community of prokaryotes and yeasts, realises stable coexistence through spatiotemporal orchestration of species and metabolite dynamics. During milk fermentation, kefir grains (a polysaccharide matrix synthesized by kefir microbes) grow in mass but remain unchanged in composition. In contrast, the milk is colonized in a sequential manner in which early members open metabolic niches for followers. Through metabolomics and large-scale mapping of inter-species interactions, we show how microbes poorly suited for milk survive in, and even dominate the community, through metabolic cooperation and uneven partitioning between grain and milk. Overall, our findings reveal how inter-species interactions partitioned in space and time lead to stable coexistence. Linked metabolomics studies:<a href='https://www.ebi.ac.uk/metabolights/MTBLS1829' rel='noopener noreferrer' target='_blank'>MTBLS1829</a> Kefir fermentation curve (FIA-MS)<a href='https://www.ebi.ac.uk/metabolights/MTBLS1830' rel='noopener noreferrer' target='_blank'>MTBLS1830</a> Interaction between the kefir isolates Lactococcus lactis and Acetobacter fabarum (GC-MS) Linked cross omic data:Genomes of isolated kefir species are available in the <a href='https://www.ncbi.nlm.nih.gov/' rel='noopener noreferrer' target='_blank'>NCBI database</a> under the accession: PRJNA375758 (bioproject ID: 375758).Metatranscriptomic sequencing reads can be accessed from <a href='www.ebi.ac.uk/ena' rel='noopener noreferrer' target='_blank'>ENA</a> under the project id PRJEB37001.Genome-scale metabolic models for kefir bacteria can be found at github.com/cdanielmachado/kefir_models.

Project description:Microbial communities in marine oxygen deficient zones (ODZs) are responsible for up to half of marine N loss through conversion of nutrients to N2O and N2. This N loss is accomplished by a consortium of diverse microbes, many of which remain uncultured. Here, we characterize genes for all steps in the anoxic N cycle in metagenomes from the water column and >30 μm particles from the Eastern Tropical North Pacific (ETNP) ODZ. We use an approach that allows for both phylogenetic identification and semi-quantitative assessment of gene abundances from individual organisms, and place these results in context of chemical measurements and rate data from the same location. Denitrification genes were enriched in >30 μm particles, even in the oxycline, while anammox bacteria were not abundant on particles. Many steps in denitrification were encoded by multiple phylotypes with different distributions. Notably three N2O reductases (nosZ), each with no cultured relative, inhabited distinct niches; one was free-living, one dominant on particles and one had a C terminal extension found in autotrophic S-oxidizing bacteria. At some depths >30% of the community possessed nitrite reductase nirK. A nirK OTU linked to SAR11 explained much of this abundance. The only bacterial gene found for NO reduction to N2O in the ODZ was a form of qnorB related to the previously postulated "nitric oxide dismutase," hypothesized to produce N2 directly while oxidizing methane. However, similar qnorB-like genes are also found in the published genomes of many bacteria that do not oxidize methane, and here the qnorB-like genes did not correlate with the presence of methane oxidation genes. Correlations with N2O concentrations indicate that these qnorB-like genes likely facilitate NO reduction to N2O in the ODZ. In the oxycline, qnorB-like genes were not detected in the water column, and estimated N2O production rates from ammonia oxidation were insufficient to support the observed oxycline N2O maximum. However, both qnorB-like and nosZ genes were present within particles in the oxycline, suggesting a particulate source of N2O and N2. Together, our analyses provide a holistic view of the diverse players in the low oxygen nitrogen cycle.

Dataset Information

Metabolic cooperation and spatiotemporal niche partitioning in a kefir microbial community.

Publications

Metabolic cooperation and spatiotemporal niche partitioning in a kefir microbial community.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets