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Migration Rates on Swim Plates Vary between Escherichia coli Soil Isolates: Differences Are Associated with Variants in Metabolic Genes

This study investigates migration phenotypes of 265 Escherichia coli soil isolates from the Buffalo River basin in Minnesota, USA. Migration rates on semisolid tryptone swim plates ranged from nonmotile to 190% of the migration rate of a highly motile E. coli K-12 strain. The nonmotile isolate, LGE0...

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Published in:Applied and environmental microbiology 2023-02, Vol.89 (2), p.e0172722-e0172722
Main Authors: Prüß, Birgit M, Horne, Shelley M, Bauer, Erika Shay, Pirner, Collin, Schwartz, Madelyn, Petersen, Morgan L, Bergholz, Peter W
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description This study investigates migration phenotypes of 265 Escherichia coli soil isolates from the Buffalo River basin in Minnesota, USA. Migration rates on semisolid tryptone swim plates ranged from nonmotile to 190% of the migration rate of a highly motile E. coli K-12 strain. The nonmotile isolate, LGE0550, had mutations in flagellar and chemotaxis genes, including two IS elements in the flagellin-encoding gene . A genome-wide association study (GWAS), associating the migration rates with genetic variants in specific genes, yielded two metabolic variants ( - and - ) with previous implications in chemotaxis. As a novel way of confirming GWAS results, we used minimal medium swim plates to confirm the associations. Other variants in metabolic genes and genes that are associated with biofilm were positively or negatively associated with migration rates. A determination of growth phenotypes on Biolog EcoPlates yielded differential growth for the 10 tested isolates on d-malic acid, putrescine, and d-xylose, all of which are important in the soil environment. E. coli is a Gram-negative, facultative anaerobic bacterium whose life cycle includes extra host environments in addition to human, animal, and plant hosts. The bacterium has the genomic capability of being motile. In this context, the significance of this study is severalfold: (i) the great diversity of migration phenotypes that we observed within our isolate collection supports previous (G. NandaKafle, A. A. Christie, S. Vilain, and V. S. Brözel, Front Microbiol 9:762, 2018, https://doi.org/10.3389/fmicb.2018.00762; Y. Somorin, F. Abram, F. Brennan, and C. O'Byrne, Appl Environ Microbiol 82:4628-4640, 2016, https://doi.org/10.1128/AEM.01175-16) ideas of soil promoting phenotypic heterogeneity, (ii) such heterogeneity may facilitate bacterial growth in the many different soil niches, and (iii) such heterogeneity may enable the bacteria to interact with human, animal, and plant hosts.
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Migration rates on semisolid tryptone swim plates ranged from nonmotile to 190% of the migration rate of a highly motile E. coli K-12 strain. The nonmotile isolate, LGE0550, had mutations in flagellar and chemotaxis genes, including two IS elements in the flagellin-encoding gene . A genome-wide association study (GWAS), associating the migration rates with genetic variants in specific genes, yielded two metabolic variants ( - and - ) with previous implications in chemotaxis. As a novel way of confirming GWAS results, we used minimal medium swim plates to confirm the associations. Other variants in metabolic genes and genes that are associated with biofilm were positively or negatively associated with migration rates. A determination of growth phenotypes on Biolog EcoPlates yielded differential growth for the 10 tested isolates on d-malic acid, putrescine, and d-xylose, all of which are important in the soil environment. E. coli is a Gram-negative, facultative anaerobic bacterium whose life cycle includes extra host environments in addition to human, animal, and plant hosts. The bacterium has the genomic capability of being motile. In this context, the significance of this study is severalfold: (i) the great diversity of migration phenotypes that we observed within our isolate collection supports previous (G. NandaKafle, A. A. Christie, S. Vilain, and V. S. Brözel, Front Microbiol 9:762, 2018, https://doi.org/10.3389/fmicb.2018.00762; Y. Somorin, F. Abram, F. Brennan, and C. 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E. coli is a Gram-negative, facultative anaerobic bacterium whose life cycle includes extra host environments in addition to human, animal, and plant hosts. The bacterium has the genomic capability of being motile. In this context, the significance of this study is severalfold: (i) the great diversity of migration phenotypes that we observed within our isolate collection supports previous (G. NandaKafle, A. A. Christie, S. Vilain, and V. S. Brözel, Front Microbiol 9:762, 2018, https://doi.org/10.3389/fmicb.2018.00762; Y. Somorin, F. Abram, F. Brennan, and C. O'Byrne, Appl Environ Microbiol 82:4628-4640, 2016, https://doi.org/10.1128/AEM.01175-16) ideas of soil promoting phenotypic heterogeneity, (ii) such heterogeneity may facilitate bacterial growth in the many different soil niches, and (iii) such heterogeneity may enable the bacteria to interact with human, animal, and plant hosts.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>36695629</pmid><doi>10.1128/aem.01727-22</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0002-5244-766X</orcidid><oa>free_for_read</oa></addata></record>
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subjects Animals
Base Composition
Biofilms
Cell migration
Chemotaxis
E coli
Environmental Microbiology
Escherichia coli
Escherichia coli Proteins - genetics
Evolution
Flagella
Flagellin
Genes
Genetic diversity
Genetic variance
Genome-wide association studies
Genome-Wide Association Study
Genomes
Humans
Malic acid
Metabolism
Mutation
Phenotypes
Phylogeny
Plates
Putrescine
River basins
RNA, Ribosomal, 16S
Semisolids
Sequence Analysis, DNA
Soil
Soil environment
Soil isolates
Soils
title Migration Rates on Swim Plates Vary between Escherichia coli Soil Isolates: Differences Are Associated with Variants in Metabolic Genes
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