Gene Expansion and Positive Selection as Bacterial Adaptations to Oligotrophic Conditions

ABSTRACT We examined the genomic adaptations of prevalent bacterial taxa in a highly nutrient- and ion-depleted freshwater environment located in the secondary cooling water system of a nuclear research reactor. Using genome-centric metagenomics, we found that none of the prevalent bacterial taxa we...

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Autores principales:	Ruben Props, Pieter Monsieurs, Peter Vandamme, Natalie Leys, Vincent J. Denef, Nico Boon
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	genomic adaptations microbial ecology oligotrophy selection streamlining Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ac41ace448a142b7a558f20c62d85459
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spelling	oai:doaj.org-article:ac41ace448a142b7a558f20c62d854592021-11-15T15:22:04ZGene Expansion and Positive Selection as Bacterial Adaptations to Oligotrophic Conditions10.1128/mSphereDirect.00011-192379-5042https://doaj.org/article/ac41ace448a142b7a558f20c62d854592019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphereDirect.00011-19https://doaj.org/toc/2379-5042ABSTRACT We examined the genomic adaptations of prevalent bacterial taxa in a highly nutrient- and ion-depleted freshwater environment located in the secondary cooling water system of a nuclear research reactor. Using genome-centric metagenomics, we found that none of the prevalent bacterial taxa were related to typical freshwater bacterial lineages. We also did not identify strong signatures of genome streamlining, which has been shown to be one of the ecoevolutionary forces shaping the genome characteristics of bacterial taxa in nutrient-depleted environments. Instead, focusing on the dominant taxon, a novel Ramlibacter sp. which we propose to name Ramlibacter aquaticus, we detected extensive positive selection on genes involved in phosphorus and carbon scavenging pathways. These genes were involved in the high-affinity phosphate uptake and storage into polyphosphate granules, metabolism of nitrogen-rich organic matter, and carbon/energy storage into polyhydroxyalkanoate. In parallel, comparative genomics revealed a high number of paralogs and an accessory genome significantly enriched in environmental sensing pathways (i.e., chemotaxis and motility), suggesting extensive gene expansions in R. aquaticus. The type strain of R. aquaticus (LMG 30558T) displayed optimal growth kinetics and productivity at low nutrient concentrations, as well as substantial cell size plasticity. Our findings with R. aquaticus LMG 30558T demonstrate that positive selection and gene expansions may represent successful adaptive strategies to oligotrophic environments that preserve high growth rates and cellular productivity. IMPORTANCE By combining a genome-centric metagenomic approach with a culture-based approach, we investigated the genomic adaptations of prevalent populations in an engineered oligotrophic freshwater system. We found evidence for widespread positive selection on genes involved in phosphorus and carbon scavenging pathways and for gene expansions in motility and environmental sensing to be important genomic adaptations of the abundant taxon in this system. In addition, microscopic and flow cytometric analysis of the first freshwater representative of this population (Ramlibacter aquaticus LMG 30558T) demonstrated phenotypic plasticity, possibly due to the metabolic versatility granted by its larger genome, to be a strategy to cope with nutrient limitation. Our study clearly demonstrates the need for the use of a broad set of genomic tools combined with culture-based physiological characterization assays to investigate and validate genomic adaptations.Ruben PropsPieter MonsieursPeter VandammeNatalie LeysVincent J. DenefNico BoonAmerican Society for Microbiologyarticlegenomic adaptationsmicrobial ecologyoligotrophyselectionstreamliningMicrobiologyQR1-502ENmSphere, Vol 4, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	genomic adaptations microbial ecology oligotrophy selection streamlining Microbiology QR1-502
spellingShingle	genomic adaptations microbial ecology oligotrophy selection streamlining Microbiology QR1-502 Ruben Props Pieter Monsieurs Peter Vandamme Natalie Leys Vincent J. Denef Nico Boon Gene Expansion and Positive Selection as Bacterial Adaptations to Oligotrophic Conditions
description	ABSTRACT We examined the genomic adaptations of prevalent bacterial taxa in a highly nutrient- and ion-depleted freshwater environment located in the secondary cooling water system of a nuclear research reactor. Using genome-centric metagenomics, we found that none of the prevalent bacterial taxa were related to typical freshwater bacterial lineages. We also did not identify strong signatures of genome streamlining, which has been shown to be one of the ecoevolutionary forces shaping the genome characteristics of bacterial taxa in nutrient-depleted environments. Instead, focusing on the dominant taxon, a novel Ramlibacter sp. which we propose to name Ramlibacter aquaticus, we detected extensive positive selection on genes involved in phosphorus and carbon scavenging pathways. These genes were involved in the high-affinity phosphate uptake and storage into polyphosphate granules, metabolism of nitrogen-rich organic matter, and carbon/energy storage into polyhydroxyalkanoate. In parallel, comparative genomics revealed a high number of paralogs and an accessory genome significantly enriched in environmental sensing pathways (i.e., chemotaxis and motility), suggesting extensive gene expansions in R. aquaticus. The type strain of R. aquaticus (LMG 30558T) displayed optimal growth kinetics and productivity at low nutrient concentrations, as well as substantial cell size plasticity. Our findings with R. aquaticus LMG 30558T demonstrate that positive selection and gene expansions may represent successful adaptive strategies to oligotrophic environments that preserve high growth rates and cellular productivity. IMPORTANCE By combining a genome-centric metagenomic approach with a culture-based approach, we investigated the genomic adaptations of prevalent populations in an engineered oligotrophic freshwater system. We found evidence for widespread positive selection on genes involved in phosphorus and carbon scavenging pathways and for gene expansions in motility and environmental sensing to be important genomic adaptations of the abundant taxon in this system. In addition, microscopic and flow cytometric analysis of the first freshwater representative of this population (Ramlibacter aquaticus LMG 30558T) demonstrated phenotypic plasticity, possibly due to the metabolic versatility granted by its larger genome, to be a strategy to cope with nutrient limitation. Our study clearly demonstrates the need for the use of a broad set of genomic tools combined with culture-based physiological characterization assays to investigate and validate genomic adaptations.
format	article
author	Ruben Props Pieter Monsieurs Peter Vandamme Natalie Leys Vincent J. Denef Nico Boon
author_facet	Ruben Props Pieter Monsieurs Peter Vandamme Natalie Leys Vincent J. Denef Nico Boon
author_sort	Ruben Props
title	Gene Expansion and Positive Selection as Bacterial Adaptations to Oligotrophic Conditions
title_short	Gene Expansion and Positive Selection as Bacterial Adaptations to Oligotrophic Conditions
title_full	Gene Expansion and Positive Selection as Bacterial Adaptations to Oligotrophic Conditions
title_fullStr	Gene Expansion and Positive Selection as Bacterial Adaptations to Oligotrophic Conditions
title_full_unstemmed	Gene Expansion and Positive Selection as Bacterial Adaptations to Oligotrophic Conditions
title_sort	gene expansion and positive selection as bacterial adaptations to oligotrophic conditions
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/ac41ace448a142b7a558f20c62d85459
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Gene Expansion and Positive Selection as Bacterial Adaptations to Oligotrophic Conditions

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