Production of the plant hormone auxin by Salmonella and its role in the interactions with plants and animals

Authors: COX, CLAYTON - University Of Florida; Brandl, Maria; DE MORAES, MARCOS - University Of Florida; GUNASEKERA, SARATH - Smithsonian Institute; TEPLITSKI, MAX - University Of Florida

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/21/2017
Publication Date: 1/12/2018
Citation: Cox, C.E., Brandl, M., De Moraes, M.H., Gunasekera, S.P., Teplitski, M. 2018. Production of the plant hormone auxin by Salmonella and its role in the interactions with plants and animals. Frontiers in Microbiology. 8:2668. https://doi.org/10.3389/fmicb.2017.02668.
DOI: https://doi.org/10.3389/fmicb.2017.02668

Interpretive Summary: The ability of foodborne pathogens to colonize plants and use them as alternate hosts is now well established. Salmonella enterica, similarly to other bacterial colonizers of plants, appears to be capable of producing the plant hormone auxin (IAA) via IpdC, an indole pyruvate (IPyA) decarboxylase. Deletion of the ipdC gene in S. enterica significantly reduced production of auxin in liquid cultures. Several lines of evidence support the hypothesis that auxin is produced by Salmonella on plants; 1) the ipdC gene was expressed on root surfaces of Medicago truncatula; 2) IAA produced by Salmonella in the M. trunculata rhizosphere activated the plant auxin-responsive gh3:gus reporter and caused an increase in secondary root formation; and 3) the wild type Salmonella cells formed aggregates at sites of lateral root emergence. On the contrary, cells of the ipdC mutant were evenly distributed in the plant rhizosphere, suggesting that IAA is involved in the aggregative behavior of Salmonella during root colonization. The ipdC mutant was also less virulent in a murine model of infection. Whereas the mutant was as proficient as the wild type strain in colonization of the mouse intestine, it was severely defective in the ability to cross the intestinal barrier. Significantly fewer cells of the ipdC mutant were detected in Peyers patches and the liver. Orthologs of ipdC are broadly distributed in Enterobacteriaceae and are present in all Salmonella genomes. Hence, the biosynthesis of IAA via IPyA in Salmonella may serve in the interaction of this human pathogen with both plant and animal hosts.

Technical Abstract: The ability of human enteric pathogens to colonize plants and use them as alternate hosts is now well established. Salmonella enterica, similarly to other phytobacteria, appears to be capable of producing the plant hormone auxin (IAA) via IpdC, an indole pyruvate (IPyA) decarboxylase. ipdC is a key gene in the IPyA pathway. Deletion of ipdC in S. enterica significantly reduced production of auxin in liquid cultures. The ipdC gene was expressed on root surfaces of Medicago truncatula. IAA produced by Salmonella in the M. trunculata rhizosphere activated the plant auxin-responsive gh3:gus reporter and caused an increase in secondary root formation. The wild type Salmonella cells formed aggregates at sites of lateral root emergence. On the contrary, cells of the ipdC mutant were evenly distributed in the plant rhizosphere, suggesting that IAA is involved in the aggregative behavior of Salmonella during root colonization. The ipdC mutant was also less virulent in a murine model of infection. Whereas it was as proficient as the wild type strain in colonization of the mouse intestine, it was severely defective in the ability to cross the intestinal barrier. Significantly fewer cells of the ipdC mutant were detected in Peyers patches and the liver. Orthologs of ipdC are broadly distributed in Enterobacteriaceae and are present in all Salmonella genomes. Hence, the biosynthesis of IAA via IPyA in Salmonella may serve in the interaction of this human pathogen with both plant and animal hosts.