Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits

ABSTRACT Much genetic diversity within a bacterial community is likely obscured by microdiversity within operational taxonomic units (OTUs) defined by 16S rRNA gene sequences. However, it is unclear how variation within this microdiversity influences ecologically relevant traits. Here, we employ a m...

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Autores principales:	Alexander B. Chase, Ulas Karaoz, Eoin L. Brodie, Zulema Gomez-Lunar, Adam C. Martiny, Jennifer B. H. Martiny
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Actinobacteria Curtobacterium Microbacteriaceae drought ecotypes glycoside hydrolases Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a4c7fd5304c74079ba1417ddd3539d8e
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spelling	oai:doaj.org-article:a4c7fd5304c74079ba1417ddd3539d8e2021-11-15T15:51:55ZMicrodiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits10.1128/mBio.01809-172150-7511https://doaj.org/article/a4c7fd5304c74079ba1417ddd3539d8e2017-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01809-17https://doaj.org/toc/2150-7511ABSTRACT Much genetic diversity within a bacterial community is likely obscured by microdiversity within operational taxonomic units (OTUs) defined by 16S rRNA gene sequences. However, it is unclear how variation within this microdiversity influences ecologically relevant traits. Here, we employ a multifaceted approach to investigate microdiversity within the dominant leaf litter bacterium, Curtobacterium, which comprises 7.8% of the bacterial community at a grassland site undergoing global change manipulations. We use cultured bacterial isolates to interpret metagenomic data, collected in situ over 2 years, together with lab-based physiological assays to determine the extent of trait variation within this abundant OTU. The response of Curtobacterium to seasonal variability and the global change manipulations, specifically an increase in relative abundance under decreased water availability, appeared to be conserved across six Curtobacterium lineages identified at this site. Genomic and physiological analyses in the lab revealed that degradation of abundant polymeric carbohydrates within leaf litter, cellulose and xylan, is nearly universal across the genus, which may contribute to its high abundance in grassland leaf litter. However, the degree of carbohydrate utilization and temperature preference for this degradation varied greatly among clades. Overall, we find that traits within Curtobacterium are conserved at different phylogenetic depths. We speculate that similar to bacteria in marine systems, diverse microbes within this taxon may be structured in distinct ecotypes that are key to understanding Curtobacterium abundance and distribution in the environment. IMPORTANCE Despite the plummeting costs of sequencing, characterizing the fine-scale genetic diversity of a microbial community—and interpreting its functional importance—remains a challenge. Indeed, most studies, particularly studies of soil, assess community composition at a broad genetic level by classifying diversity into taxa (OTUs) defined by 16S rRNA sequence similarity. However, these classifications potentially obscure variation in traits that result in fine-scale ecological differentiation among closely related strains. Here, we investigated “microdiversity” in a highly diverse and poorly characterized soil system (leaf litter in a southern Californian grassland). We focused on the most abundant bacterium, Curtobacterium, which by standard methods is grouped into only one OTU. We find that the degree of carbohydrate usage and temperature preference vary within the OTU, whereas its responses to changes in precipitation are relatively uniform. These results suggest that microdiversity may be key to understanding how soil bacterial diversity is linked to ecosystem functioning.Alexander B. ChaseUlas KaraozEoin L. BrodieZulema Gomez-LunarAdam C. MartinyJennifer B. H. MartinyAmerican Society for MicrobiologyarticleActinobacteriaCurtobacteriumMicrobacteriaceaedroughtecotypesglycoside hydrolasesMicrobiologyQR1-502ENmBio, Vol 8, Iss 6 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Actinobacteria Curtobacterium Microbacteriaceae drought ecotypes glycoside hydrolases Microbiology QR1-502
spellingShingle	Actinobacteria Curtobacterium Microbacteriaceae drought ecotypes glycoside hydrolases Microbiology QR1-502 Alexander B. Chase Ulas Karaoz Eoin L. Brodie Zulema Gomez-Lunar Adam C. Martiny Jennifer B. H. Martiny Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits
description	ABSTRACT Much genetic diversity within a bacterial community is likely obscured by microdiversity within operational taxonomic units (OTUs) defined by 16S rRNA gene sequences. However, it is unclear how variation within this microdiversity influences ecologically relevant traits. Here, we employ a multifaceted approach to investigate microdiversity within the dominant leaf litter bacterium, Curtobacterium, which comprises 7.8% of the bacterial community at a grassland site undergoing global change manipulations. We use cultured bacterial isolates to interpret metagenomic data, collected in situ over 2 years, together with lab-based physiological assays to determine the extent of trait variation within this abundant OTU. The response of Curtobacterium to seasonal variability and the global change manipulations, specifically an increase in relative abundance under decreased water availability, appeared to be conserved across six Curtobacterium lineages identified at this site. Genomic and physiological analyses in the lab revealed that degradation of abundant polymeric carbohydrates within leaf litter, cellulose and xylan, is nearly universal across the genus, which may contribute to its high abundance in grassland leaf litter. However, the degree of carbohydrate utilization and temperature preference for this degradation varied greatly among clades. Overall, we find that traits within Curtobacterium are conserved at different phylogenetic depths. We speculate that similar to bacteria in marine systems, diverse microbes within this taxon may be structured in distinct ecotypes that are key to understanding Curtobacterium abundance and distribution in the environment. IMPORTANCE Despite the plummeting costs of sequencing, characterizing the fine-scale genetic diversity of a microbial community—and interpreting its functional importance—remains a challenge. Indeed, most studies, particularly studies of soil, assess community composition at a broad genetic level by classifying diversity into taxa (OTUs) defined by 16S rRNA sequence similarity. However, these classifications potentially obscure variation in traits that result in fine-scale ecological differentiation among closely related strains. Here, we investigated “microdiversity” in a highly diverse and poorly characterized soil system (leaf litter in a southern Californian grassland). We focused on the most abundant bacterium, Curtobacterium, which by standard methods is grouped into only one OTU. We find that the degree of carbohydrate usage and temperature preference vary within the OTU, whereas its responses to changes in precipitation are relatively uniform. These results suggest that microdiversity may be key to understanding how soil bacterial diversity is linked to ecosystem functioning.
format	article
author	Alexander B. Chase Ulas Karaoz Eoin L. Brodie Zulema Gomez-Lunar Adam C. Martiny Jennifer B. H. Martiny
author_facet	Alexander B. Chase Ulas Karaoz Eoin L. Brodie Zulema Gomez-Lunar Adam C. Martiny Jennifer B. H. Martiny
author_sort	Alexander B. Chase
title	Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits
title_short	Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits
title_full	Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits
title_fullStr	Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits
title_full_unstemmed	Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits
title_sort	microdiversity of an abundant terrestrial bacterium encompasses extensive variation in ecologically relevant traits
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/a4c7fd5304c74079ba1417ddd3539d8e
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Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits

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