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

Abstract

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. Wemore » 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.« less

Authors:
; ORCiD logo; ; ; ; ;
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1437767
Alternate Identifier(s):
OSTI ID: 1432219
Grant/Contract Number:  
SC-SC0016410; PS02-09ER09-25; AC02-05CH11231; SC0016410
Resource Type:
Journal Article: Published Article
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online) Journal Volume: 8 Journal Issue: 6; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Actinobacteria; Curtobacterium; Microbacteriaceae; drought; ecotypes; glycoside hydrolases; nitrogen addition

Citation Formats

Chase, Alexander B., Karaoz, Ulas, Brodie, Eoin L., Gomez-Lunar, Zulema, Martiny, Adam C., Martiny, Jennifer B. H., and Zhou, ed., Jizhong. Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits. United States: N. p., 2017. Web. doi:10.1128/mBio.01809-17.
Chase, Alexander B., Karaoz, Ulas, Brodie, Eoin L., Gomez-Lunar, Zulema, Martiny, Adam C., Martiny, Jennifer B. H., & Zhou, ed., Jizhong. Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits. United States. doi:10.1128/mBio.01809-17.
Chase, Alexander B., Karaoz, Ulas, Brodie, Eoin L., Gomez-Lunar, Zulema, Martiny, Adam C., Martiny, Jennifer B. H., and Zhou, ed., Jizhong. Tue . "Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits". United States. doi:10.1128/mBio.01809-17.
@article{osti_1437767,
title = {Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits},
author = {Chase, Alexander B. and Karaoz, Ulas and Brodie, Eoin L. and Gomez-Lunar, Zulema and Martiny, Adam C. and Martiny, Jennifer B. H. and Zhou, ed., Jizhong},
abstractNote = {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.},
doi = {10.1128/mBio.01809-17},
journal = {mBio (Online)},
issn = {2150-7511},
number = 6,
volume = 8,
place = {United States},
year = {2017},
month = {11}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1128/mBio.01809-17

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Cited by: 7 works
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    Works referencing / citing this record:

    Construction and Characterization of Synthetic Bacterial Community for Experimental Ecology and Evolution
    journal, August 2018