Ecological Conditions and Molecular Determinants Involved in Agrobacterium Lifestyle in Tumors

Abstract

The study of pathogenic agents in their natural niches allows for a better understanding of disease persistence and dissemination. Bacteria belonging to the Agrobacterium genus are soil-borne and can colonize the rhizosphere. These bacteria are also well known as phytopathogens as they can cause tumors (crown gall disease) by transferring a DNA region (T-DNA) into a wide range of plants. Most reviews on Agrobacterium are focused on virulence determinants, T-DNA integration, bacterial and plant factors influencing the efficiency of genetic transformation. Recent research papers have focused on the plant tumor environment on the one hand, and genetic traits potentially involved in bacterium-plant interactions on the other hand. The present review gathers current knowledge about the special conditions encountered in the tumor environment along with the Agrobacterium genetic determinants putatively involved in bacterial persistence inside a tumor. By integrating recent metabolomic and transcriptomic studies, we describe how tumors develop and how Agrobacterium can maintain itself in this nutrient-rich but stressful and competitive environment.

Phenotypic and Molecular-Phylogenetic Analyses Reveal Distinct Features of Crown Gall-Associated Xanthomonas Strains

“…A physiologically active crown gall produces specific nutrients (opines) utilizable by microorganisms, providing a rich niche for plant-associated bacteria to colonize, grow, and form complex ecological interactions ( 34 – 37 ). The microbial communities involved in opine ecology are not limited to Agrobacterium members.…”

“…The genome of Pseudomonas kilonensis strain 1855-344, which can catabolize octopine, was recently shown to contain an octopine-catabolic operon named ooxAB ( 40 ). Successful colonization and long-term persistence of Agrobacterium strains on/in crown gall tissue depend partly on competition for opine nutritive resources, either between the agrobacteria or among other microorganisms, such as pseudomonads, Sinorhizobium spp., coryneform bacteria, or even fungal species such as Cylindrocarpon heteronema and Fusarium solani ( 36 , 37 ). It was recently shown that the microbial community of natural grapevine ( Vitis vinifera ) crown galls caused by Allorhizobium vitis contains more than 150 bacterial species, among which members of Pseudomonas , Sphingomonas , and Erwinia were more common ( 38 ).…”

“…It was recently shown that the microbial community of natural grapevine ( Vitis vinifera ) crown galls caused by Allorhizobium vitis contains more than 150 bacterial species, among which members of Pseudomonas , Sphingomonas , and Erwinia were more common ( 38 ). Furthermore, crown galls can harbor bacteria belonging to Corynebacterium or Arthrobacter ( 37 ). The abundance of A. vitis in grapevine crown gall is positively correlated with the abundance of Novosphingobium sp., Xanthomonas sp., and members of Microbacteriaceae , suggesting the presence of a microbial hub in the crown gall environment ( 3 ).…”

Rhizobiales -Specific RirA Represses a Naturally “Synthetic” Foreign Siderophore Gene Cluster To Maintain Sinorhizobium -Legume Mutualism

“…Transcriptomic and/or phenotypic characterizations of the rirA mutant have demonstrated RirA as an iron-responsive regulator under free-living conditions in R. leguminosarum ( 26 , 32 ), Sinorhizobium meliloti ( 33 – 35 ), Sinorhizobium fredii ( 36 ), and Agrobacterium tumefaciens ( 25 , 37 ). RirA is required for pathogenesis of A. tumefaciens on tobacco leaves ( 37 , 38 ). Symbiotic defects were not observed for the rirA mutants of R. leguminosarum ( 26 ) and S. meliloti ( 33 ), both of which undergo irreversible terminal differentiation (impaired reproductive ability) in nodule cells of pea and alfalfa, respectively ( 39 , 40 ).…”

Reconstruction and analysis of a genome‐scale metabolic model for Agrobacterium tumefaciens

“…Genetic transformation by A. tumefaciens is related to its pathogenicity and involves a shift from free‐living to plant‐associated forms. Soilborne A. tumefaciens is widely found in natural habitats, such as the bulk soil and rhizosphere (Meyer et al, 2019), where it is subjected to nutrient limitation and external stress, including pollutants. On sensing phenols and other nutrients secreted from plant wounds, A. tumefaciens moves to wound sites and mediates crown gall formation to create a better environment for survival.…”