Genetic and Functional Diversity Help Explain Pathogenic, Weakly Pathogenic, and Commensal Lifestyles in the Genus Xanthomonas

Pena, Michelle M.; Bhandari, Rishi; Bowers, Robert M.; Weis, Kylie; Newberry, Eric; Wagner, Naama; Pupko, Tal; Jones, Jeffrey B.; Woyke, Tanja; Vinatzer, Boris A.; Jacques, Marie-Agnès; Potnis, Neha

doi:10.1093/gbe/evae074

Title: Genetic and Functional Diversity Help Explain Pathogenic, Weakly Pathogenic, and Commensal Lifestyles in the Genus Xanthomonas

Journal Article · 22 April 2024 · Genome Biology and Evolution

DOI: https://doi.org/10.1093/gbe/evae074 · OSTI ID:2396672

Pena, Michelle M. ^[1]; Bhandari, Rishi ^[2]; Bowers, Robert M. ^[3]; Weis, Kylie ^[2]; Newberry, Eric ^[2];

^[4];

^[5]; Jones, Jeffrey B. ^[6]; Woyke, Tanja ^[7];

^[8]; Jacques, Marie-Agnès ^[9]; Potnis, Neha ^[2]

Auburn Univ., AL (United States); Univ. of Georgia, Tifton, GA (United States)
Auburn Univ., AL (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Tel Aviv Univ., Tel Aviv (Israel)
Tel Aviv Univ., Tel Aviv (Israel)
Univ. of Florida, Gainesville, FL (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Univ. of California, Merced, CA (United States)
Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States)
Univ. of Angers (France)

The genus Xanthomonas has been primarily studied for pathogenic interactions with plants. However, besides host and tissue-specific pathogenic strains, this genus also comprises nonpathogenic strains isolated from a broad range of hosts, sometimes in association with pathogenic strains, and other environments, including rainwater. Based on their incapacity or limited capacity to cause symptoms on the host of isolation, nonpathogenic xanthomonads can be further characterized as commensal and weakly pathogenic. This study aimed to understand the diversity and evolution of nonpathogenic xanthomonads compared to their pathogenic counterparts based on their cooccurrence and phylogenetic relationship and to identify genomic traits that form the basis of a life history framework that groups xanthomonads by ecological strategies. We sequenced genomes of 83 strains spanning the genus phylogeny and identified eight novel species, indicating unexplored diversity. While some nonpathogenic species have experienced a recent loss of a type III secretion system, specifically the hrp2 cluster, we observed an apparent lack of association of the hrp2 cluster with lifestyles of diverse species. We performed association analysis on a large data set of 337 Xanthomonas strains to explain how xanthomonads may have established association with the plants across the continuum of lifestyles from commensals to weak pathogens to pathogens. Presence of distinct transcriptional regulators, distinct nutrient utilization and assimilation genes, transcriptional regulators, and chemotaxis genes may explain lifestyle-specific adaptations of xanthomonads.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2396672

Journal Information:: Genome Biology and Evolution, Journal Name: Genome Biology and Evolution Journal Issue: 4 Vol. 16; ISSN 1759-6653

Publisher:: Society for Molecular Biology and EvolutionCopyright Statement

Country of Publication:: United States

Language:: English

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Novel Xanthomonas Species From the Perennial Ryegrass Seed Microbiome – Assessing the Bioprotection Activity of Non-pathogenic Relatives of Pathogens Li, Tongda; Mann, Ross; Sawbridge, Timothy Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.01991	journal	August 2020
Phylogenetic Distribution and Evolution of Type VI Secretion System in the Genus Xanthomonas Liyanapathiranage, Prabha; Wagner, Naama; Avram, Oren Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.840308	journal	April 2022
What makes Xanthomonas albilineans unique amongst xanthomonads? Pieretti, Isabelle; Pesic, Alexander; Petras, Daniel Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00289	journal	April 2015
Comparative genomics of a cannabis pathogen reveals insight into the evolution of pathogenicity in Xanthomonas Jacobs, Jonathan M.; Pesce, CÃ©line; Lefeuvre, Pierre Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00431	journal	June 2015
Comparative Genomics of Pathogenic and Nonpathogenic Strains of Xanthomonas arboricola Unveil Molecular and Evolutionary Events Linked to Pathoadaptation Cesbron, Sophie; Briand, Martial; Essakhi, Salwa Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.01126	journal	December 2015
Draft Genome Sequences of Xanthomonas sacchari and Two Banana-Associated Xanthomonads Reveal Insights into the Xanthomonas Group 1 Clade Studholme, David J.; Wasukira, Arthur; Paszkiewicz, Konrad Genes, Vol. 2, Issue 4 https://doi.org/10.3390/genes2041050	journal	December 2011
Cooperative virulence via the collective action of secreted pathogen effectors Guttman, David; Ruiz-Bedoya, Tatiana; Wang, Pauline W. Zenodo https://doi.org/10.5281/zenodo.7254975	dataset	January 2022
Rapid scoring of genes in microbial pan-genome-wide association studies with Scoary Brynildsrud, Ola; Bohlin, Jon; Scheffer, Lonneke Figshare https://doi.org/10.6084/m9.figshare.c.3619730	collection	January 2016

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