Legume seed exudates and Physcomitrella patens extracts influence swarming behavior in Rhizobium leguminosarum

Abstract

Plants are known to secrete chemical compounds that can change the behavior of rhizosphere-inhabiting bacteria. We investigated the effects of extracts from legume host plants on the swarming behavior of Rhizobium leguminosarum bv. viciae. We also investigated the effects on swarming when Rhizobium is exposed to extracts from an ancestor to vascular plants, the model bryophyte Physcomitrella patens. Lentil and faba bean seed exudates enhanced and inhibited swarming motility, respectively, whereas pea seed exudates had no observable effect on swarming. Swarming was also enhanced by the moss extracts. Exposure to lentil seed exudates and the moss extract increased flaA expression 2-fold, while faba bean seed exudates exposure decreased expression 3-fold, suggesting that the swarming effect could, in part, be due to regulation of flagellin gene expression. However, the exudates and extracts did not significantly affect flaA gene expression in planktonic motile cells, indicating that the response to flagellar regulation is specific to a physiology unique to the swarming cell. Transmission electron microscopy demonstrated that addition of the lentil seed exudate and the moss extract results in earlier differentiation into swarmer cells, which could contribute to the development of a larger swarming surface area. To gain further mechanistic insight into the effect of the moss extract on swarming, a moss strigolactone-deficient mutant (Ppccd8⌬) was tested. A reduction in the promotive effect was observed, suggesting that the plant hormone strigolactone may be a signalling molecule activating swarming motility in R. leguminosarum.Key words: Rhizobium, swarming motility, plant extracts. Résumé :Les plantes sont reconnues pour sécréter des composés chimiques qui modifient le comportement des bactéries vivant en rhizosphère. Nous avons examiné l'impact d'extraits de plantes légumineuses hôtes sur l'essaimage de Rhizobium leguminosarum bv. viciae. Nous avons également examiné la modulation de l'essaimage lorsque Rhizobium était exposé à des extraits d'un ancêtre des plantes vasculaires, la bryophyte modèle Physcomitrella patens. Des exsudats de graines de lentille et de féveroles ont respectivement stimulé et inhibé l'essaimage, alors que des exsudats de graines de pois n'ont pas eu d'effet notable. L'essaimage a aussi été stimulé par des extraits de mousse. L'exposition aux exsudats de graines de lentille et à l'extrait de mousse a doublé l'expression de flaA alors que les exsudats de graines de féveroles l'ont diminué des deux tiers, ce qui indique que l'effet sur l'essaimage pourrait être partiellement attribuable à la régulation de l'expression du gène de la flagelline. Or, les exsudats et extraits n'ont pas eu d'incidence significative sur l'expression du gène flaA chez les cellules planctoniques motiles, ce qui indique que la réponse en termes de régulation flagellaire n'opérerait que grâce à une physiologie particulière de la cellule en essaimage. La microscopie électronique par transmission a démontré que ...

Adaptation Mechanisms in the Evolution of Moss Defenses to Microbes

“…The moss Physcomitrella patens ( P. patens ) produces chemical compounds that increase swarming of Rhizobium leguminosarum , which is a process of rapid and coordinated movement of bacteria leading to rhizosphere colonization (Tambalo et al, 2014). Movement is probably related to increased expression of genes involved in flagellar filament formation and motility.…”

“…Bacterial swarming behavior can be influenced by plant strigolactone, since extracts of a strigolactone-deficient moss mutant induce less swarming motility in R. leguminosarum . Accordingly, the existence of beneficial interactions between moss and rhizobia, suggest a potential ancient signal perception mechanism between these type of bacteria and plants (Tambalo et al, 2014). Studies of moss-associated bacteria in different ecosystems have shown the presence of diverse microbial populations with a high proportion of antagonistic isolates to fungal pathogens, suggesting that mosses harbor bacteria with antifungal activities that contribute to plant defense (Opelt et al, 2007a,b).…”

Seeds integrate biological information about conspecific and allospecific neighbours

“…To identify possible cues, we tested the following: (i) sibling seed þ DW (control), (ii) non-sibling seed þ 100 ). Each 124 extract was derived from a single seed with no visible cracks (a commonly used approach to collect of seed extract [19,20]). If discrimination of the presence of seeds of another species depends on water-soluble chemicals, then seeds in ST5 will germinate faster than those in the sibling condition and faster than or in synchrony with those in the NST5 condition.…”

Strigolactones in the Rhizosphere: Friend or Foe?

“…However, the crystal structure of the rice strigolactone receptor D14 resembles that of the Bacillus subtilis RsbQ protein that is a stress-response regulator with hydrolase activity (Kagiyama et al 2013), indicating that strigolactones might influence rhizobial cellular activity in a manner different from that tested above. Indeed, a role for strigolactones has been implied in the chemical dialog between plants and rhizobia (Peláez-Vico et al 2016;Tambalo et al 2014). For instance, extracts of the moss Physcomitrella patens stimulate the swarming motility, i.e., a rapid coordinated movement of bacteria across a surface, in Rhizobium leguminosarum, whereas this promoting effect is reduced by extracts from the strigolactone-deficient strain Physcomitrella patens Ppccd8D (Peláez-Vico et al 2016;Tambalo et al 2014).…”

“…Indeed, a role for strigolactones has been implied in the chemical dialog between plants and rhizobia (Peláez-Vico et al 2016;Tambalo et al 2014). For instance, extracts of the moss Physcomitrella patens stimulate the swarming motility, i.e., a rapid coordinated movement of bacteria across a surface, in Rhizobium leguminosarum, whereas this promoting effect is reduced by extracts from the strigolactone-deficient strain Physcomitrella patens Ppccd8D (Peláez-Vico et al 2016;Tambalo et al 2014). In addition, rac-GR24 triggers the swarming motility of Sinorhizobium meliloti in a dose-dependent manner (Peláez-Vico et al 2016).…”