Genome-Wide Comparative Functional Analyses Reveal Adaptations of Salmonella sv. Newport to a Plant Colonization Lifestyle

Outbreaks of salmonellosis linked to the consumption of vegetables have been disproportionately associated with strains of serovar Newport. We tested the hypothesis that strains of sv. Newport have evolved unique adaptations to persistence in plants that are not shared by strains of other Salmonella...

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Main Authors: Marcos H. de Moraes, Emanuel Becerra Soto, Isai Salas González, Prerak Desai, Weiping Chu, Steffen Porwollik, Michael McClelland, Max Teplitski
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-05-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2018.00877/full
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spelling doaj-51b19a59eaa248fd831b982fdc5ee1ee2020-11-25T00:15:19ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-05-01910.3389/fmicb.2018.00877344523Genome-Wide Comparative Functional Analyses Reveal Adaptations of Salmonella sv. Newport to a Plant Colonization LifestyleMarcos H. de Moraes0Emanuel Becerra Soto1Isai Salas González2Isai Salas González3Isai Salas González4Prerak Desai5Weiping Chu6Steffen Porwollik7Michael McClelland8Max Teplitski9Soil and Water Sciences Department, University of Florida, Gainesville, FL, United StatesCenter for Genomic Sciences, National Autonomous University of Mexico, Cuernavaca, MexicoCenter for Genomic Sciences, National Autonomous University of Mexico, Cuernavaca, MexicoDepartment of Biology, The University of North Carolina at Chapel Hill, Chapel Hill, NC, United StatesCurriculum in Bioinformatics and Computational Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC, United StatesDepartment of Microbiology and Molecular Genetics, University of California, Irvine, Irvine, CA, United StatesDepartment of Microbiology and Molecular Genetics, University of California, Irvine, Irvine, CA, United StatesDepartment of Microbiology and Molecular Genetics, University of California, Irvine, Irvine, CA, United StatesDepartment of Microbiology and Molecular Genetics, University of California, Irvine, Irvine, CA, United StatesSoil and Water Sciences Department, University of Florida, Gainesville, FL, United StatesOutbreaks of salmonellosis linked to the consumption of vegetables have been disproportionately associated with strains of serovar Newport. We tested the hypothesis that strains of sv. Newport have evolved unique adaptations to persistence in plants that are not shared by strains of other Salmonella serovars. We used a genome-wide mutant screen to compare growth in tomato fruit of a sv. Newport strain from an outbreak traced to tomatoes, and a sv. Typhimurium strain from animals. Most genes in the sv. Newport strain that were selected during persistence in tomatoes were shared with, and similarly selected in, the sv. Typhimurium strain. Many of their functions are linked to central metabolism, including amino acid biosynthetic pathways, iron acquisition, and maintenance of cell structure. One exception was a greater need for the core genes involved in purine metabolism in sv. Typhimurium than in sv. Newport. We discovered a gene, papA, that was unique to sv. Newport and contributed to the strain’s fitness in tomatoes. The papA gene was present in about 25% of sv. Newport Group III genomes and generally absent from other Salmonella genomes. Homologs of papA were detected in the genomes of Pantoea, Dickeya, and Pectobacterium, members of the Enterobacteriacea family that can colonize both plants and animals.https://www.frontiersin.org/article/10.3389/fmicb.2018.00877/fulltomatoplant-microbe interactionscomparative genomicspan-genomevegetable safety
collection DOAJ
language English
format Article
sources DOAJ
author Marcos H. de Moraes
Emanuel Becerra Soto
Isai Salas González
Isai Salas González
Isai Salas González
Prerak Desai
Weiping Chu
Steffen Porwollik
Michael McClelland
Max Teplitski
spellingShingle Marcos H. de Moraes
Emanuel Becerra Soto
Isai Salas González
Isai Salas González
Isai Salas González
Prerak Desai
Weiping Chu
Steffen Porwollik
Michael McClelland
Max Teplitski
Genome-Wide Comparative Functional Analyses Reveal Adaptations of Salmonella sv. Newport to a Plant Colonization Lifestyle
Frontiers in Microbiology
tomato
plant-microbe interactions
comparative genomics
pan-genome
vegetable safety
author_facet Marcos H. de Moraes
Emanuel Becerra Soto
Isai Salas González
Isai Salas González
Isai Salas González
Prerak Desai
Weiping Chu
Steffen Porwollik
Michael McClelland
Max Teplitski
author_sort Marcos H. de Moraes
title Genome-Wide Comparative Functional Analyses Reveal Adaptations of Salmonella sv. Newport to a Plant Colonization Lifestyle
title_short Genome-Wide Comparative Functional Analyses Reveal Adaptations of Salmonella sv. Newport to a Plant Colonization Lifestyle
title_full Genome-Wide Comparative Functional Analyses Reveal Adaptations of Salmonella sv. Newport to a Plant Colonization Lifestyle
title_fullStr Genome-Wide Comparative Functional Analyses Reveal Adaptations of Salmonella sv. Newport to a Plant Colonization Lifestyle
title_full_unstemmed Genome-Wide Comparative Functional Analyses Reveal Adaptations of Salmonella sv. Newport to a Plant Colonization Lifestyle
title_sort genome-wide comparative functional analyses reveal adaptations of salmonella sv. newport to a plant colonization lifestyle
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2018-05-01
description Outbreaks of salmonellosis linked to the consumption of vegetables have been disproportionately associated with strains of serovar Newport. We tested the hypothesis that strains of sv. Newport have evolved unique adaptations to persistence in plants that are not shared by strains of other Salmonella serovars. We used a genome-wide mutant screen to compare growth in tomato fruit of a sv. Newport strain from an outbreak traced to tomatoes, and a sv. Typhimurium strain from animals. Most genes in the sv. Newport strain that were selected during persistence in tomatoes were shared with, and similarly selected in, the sv. Typhimurium strain. Many of their functions are linked to central metabolism, including amino acid biosynthetic pathways, iron acquisition, and maintenance of cell structure. One exception was a greater need for the core genes involved in purine metabolism in sv. Typhimurium than in sv. Newport. We discovered a gene, papA, that was unique to sv. Newport and contributed to the strain’s fitness in tomatoes. The papA gene was present in about 25% of sv. Newport Group III genomes and generally absent from other Salmonella genomes. Homologs of papA were detected in the genomes of Pantoea, Dickeya, and Pectobacterium, members of the Enterobacteriacea family that can colonize both plants and animals.
topic tomato
plant-microbe interactions
comparative genomics
pan-genome
vegetable safety
url https://www.frontiersin.org/article/10.3389/fmicb.2018.00877/full
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