Incidences of bacterial foodborne illness caused by ingestion of fresh produce are rising. Instead of this being due to incidental contamination, the animal pathogen Salmonella enterica utilizes specific molecular mechanisms to attach to and colonize plants. This work characterizes two S. enterica genes of unknown function: a putative periplasmic protein, STM0278, and a putative protein with a hydrolase in the C-terminus, STM0650. STM0278 and STM0650 are important for seedling colonization but appear to have different roles during the process of colonization. Mutants of either STM0278 or STM0650 showed reduced colonization of alfalfa seedlings at 24 h, and the STM0278 mutant also showed reduced colonization at 48 h. Both genes were expressed in planta at 4 h following inoculation of 3-day-old seedlings and at 72 h after seed inoculation. This suggests that the role of STM0650 in seedling colonization is less important later in the process or is duplicated by other mechanisms. Mutants of STM0278 and STM0650 were defective in swarming. The STM0278 mutant failed to swarm in 24 h, while swarming of the STM0650 mutant was delayed. Addition of surfactant restored swarming of the STM0278 mutant, suggesting that STM0278 is involved in surfactant or osmotic agent production or deployment. Alfalfa seed exudates as the sole nutrient source were capable of perpetuating S. enterica swarming. Sequence analysis revealed sequences homologous to STM0278 and STM0650 in plant-associated bacteria, but none in Escherichia coli. Phylogenetic analysis of STM0650 showed similar sequences from diverse classes of plant-associated bacteria. Bacteria that preferentially colonize roots, including S. enterica, may use a similar hydrolase for swarming or biofilm production on plants. Multicellular behaviours by S. enterica appear central to plant colonization. S. enterica genes involved in plant colonization and survival outside of a host are most likely among the ‘function unknown’ genes of this bacterium.
BaisH. P.,
WeirT. L.,
PerryL. G.,
GilroyS.,
VivancoJ. M.2006; The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266
BarakJ. D.,
WhitehandL. C.,
CharkowskiA. O.2002; Differences in attachment of Salmonella enterica serovars and Escherichia coli O157 : H7 to alfalfa sprouts. Appl Environ Microbiol 68:4758–4763
BarakJ. D.,
GorskiL.,
Naraghi-AraniP.,
CharkowskiA. O.2005; Salmonella enterica virulence genes are required for bacterial attachment to plant tissue. Appl Environ Microbiol 71:5685–5691
BarakJ. D.,
JahnC. E.,
GibsonD. L.,
CharkowskiA. O.2007; The role of cellulose and O-antigen capsule in the colonization of plants by Salmonella enterica
. Mol Plant Microbe Interact 20:1083–1091
BoureauT.,
JacquesM. A.,
BerruyerR.,
DessauxY.,
DominquezH.,
MorrisC. E.2004; Comparison of the phenotypes and genotypes of biofilm and solitary epiphytic bacterial populations on broad-leaved endive. Microb Ecol 47:87–95
CharkowskiA. O.,
BarakJ. D.,
SarrealC. Z.,
MandrellR. E.2002; Differences in growth of Salmonella enterica and Escherichia coli O157 : H7 on alfalfa sprouts. Appl Environ Microbiol 68:3114–3120
CooleyM. B.,
MillerW. G.,
MandrellR. E.2003; Colonization of Arabidopsis thaliana with Salmonella enterica and enterohemorrhagic Escherichia coli O157 : H7 and competition by Enterobacter asburiae
. Appl Environ Microbiol 69:4915–4926
GorskiL.,
PalumboJ. D.,
MandrellR. E.2003; Attachment of Listeria monocytogenes to radish tissue is dependent upon temperature and flagellar motility. Appl Environ Microbiol 69:258–266
GorskiL.,
DuhãJ. M.,
FlahertyD.2009; The use of flagella and motility for plant colonization and fitness by different strains of the foodborne pathogen Listeria monocytogenes
. PLoS One 4:e5142
HarsheyR. M.,
MatsuyamaT.1994; Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells. Proc Natl Acad Sci U S A 91:8631–8635
InamiG. B.,
MolerS. E.1999; Detection and isolation of Salmonella from naturally contaminated alfalfa seeds following an outbreak investigation. J Food Prot 62:662–664
JeterC.,
MatthysseA. G.2005; Characterization of the binding of diarrheagenic strains of E. coli to plant surfaces and the role of curli in the interaction of the bacteria with alfalfa sprouts. Mol Plant Microbe Interact 18:1235–1242
KimW.,
SuretteM. G.2006; Coordinated regulation of two independent cell-cell signaling systems and swarmer differentiation in Salmonella enterica serovar Typhimurium. J Bacteriol 188:431–440
KlerksM. M.,
van Gent-PelzerM.,
FranzE.,
ZijlstraC.,
van BruggenA. H. C.2007; Physiological and molecular responses of Lactuca sativa to colonization by Salmonella enterica serovar Dublin. Appl Environ Microbiol 73:4905–4914
SmithJ. N.,
DyszelJ. L.,
SoaresJ. A.,
EllermeierC. D.,
AltierC.,
LawhonS. D.,
AdamsL. G.,
KonjufcaV.,
CurtissR.IIIother authors2008; SdiA, an N-acylhomoserine lactone receptor, becomes active during the transit of Salmonella enterica through the gastrointestinal tract of turtles. PLoS One 3:e2826