Bacillus subtilis Early Colonization of Arabidopsis thaliana Roots Involves Multiple Chemotaxis Receptors

Abstract

Colonization of plant roots by Bacillus subtilis is mutually beneficial to plants and bacteria. Plants can secrete up to 30% of their fixed carbon via root exudates, thereby feeding the bacteria, and in return the associated B. subtilis bacteria provide the plant with many growth-promoting traits. Formation of a biofilm on the root by matrix-producing B. subtilis is a well-established requirement for long-term colonization. However, we observed that cells start forming a biofilm only several hours after motile cells first settle on the plant. We also found that intact chemotaxis machinery is required for early root colonization by B. subtilis and for plant protection. Arabidopsis thaliana root exudates attract B. subtilis in vitro, an activity mediated by the two characterized chemoreceptors, McpB and McpC, as well as by the orphan receptor TlpC. Nonetheless, bacteria lacking these chemoreceptors are still able to colonize the root, suggesting that other chemoreceptors might also play a role in this process. These observations suggest that A. thaliana actively recruits B. subtilis through root-secreted molecules, and our results stress the important roles of B. subtilis chemoreceptors for efficient colonization of plants in natural environments. These results demonstrate a remarkable strategy adapted by beneficial rhizobacteria to utilize carbon-rich root exudates, which may facilitate rhizobacterial colonization and a mutualistic association with the host.

Recognition of dominant attractants by key chemoreceptors mediates recruitment of plant growth‐promoting rhizobacteria

“…Chemoreceptor‐mediated taxis to root exudates is frequently essential to initiate the interaction between plants and rhizobacteria. This is the case for symbiotic and nonsymbiotic beneficial bacteria as well as for pathogenic species (Hazelbauer and Lai, ; Hida et al, ; Allard‐Massicotte et al, ; Scharf et al, ; Matilla and Krell, ). Studies of bacterial chemotaxis to plant root exudates, as well as its role in rhizosphere colonization, have received increasing attention in recent years (Scharf et al, ; Massalha et al, ).…”

“…A parallel study using the plant‐associated B. subtilis NCIB3610 strain indicated that chemoreceptors McpB, McpC and TlpC dominate the bacterial chemotaxis to A. thaliana root exudates, while the early colonization of plant roots by B. subtilis was dependent on additional chemoreceptors (Allard‐Massicotte et al, ). In contrast, only McpA and McpC were found to be essential for root colonization by B. velezensis SQR9.…”

“…In a recent study, Allard‐Massicotte et al . () reported that chemoreceptors McpB, McpC and TlpC mediated chemotaxis of the plant‐associated strain B. subtilis 3610 to Arabidopsis thaliana root exudates and early root colonization. The oxygen sensing chemoreceptor IcpB of the plant beneficial bacterium Azorhizobium caulinodans modulated nodulation and nitrogen fixation on the stems and roots of Sesbania rostrata (Jiang et al, ).…”

“…and Bacillus subtilis (Porter et al, 2011;Bi and Lai, 2015;Sampedro et al, 2015), ecophysiological studies of different rhizobacteria have allowed the identification of plant signals that are central to colonization-relevant chemotaxis, as well as the cognate chemoreceptor. In a recent study, Allard-Massicotte et al (2016) reported that chemoreceptors McpB, McpC and TlpC mediated chemotaxis of the plant-associated strain B. subtilis 3610 to Arabidopsis thaliana root exudates and early root colonization. The oxygen sensing chemoreceptor IcpB of the plant beneficial bacterium Azorhizobium caulinodans modulated nodulation and nitrogen fixation on the stems and roots of Sesbania rostrata (Jiang et al, 2016).…”

Plant root exudation under drought: implications for ecosystem functioning

“…For example, drought increased organic acid exudation in maize, particularly of malic acid (along with fumaric, malonic, succinic and oxalic acids; Henry et al , ), which is an effective chemoattractant for Bacillus subtilis (e.g. in the soybean rhizosphere; Allard‐Massicotte et al , ). B. subtilis is a beneficial bacterial species that increases drought resistance in Phleum pratense L. by activating osmolyte secretion (Gagné‐Bourque et al , ).…”