Abstract
Bacteria form biofilms as a means to adapt to environmental changes for survival. Pellicle is a floating biofilm formed at the air–liquid interface in static culture conditions; however, its functional roles have received relatively little attention compared to solid surface-associated biofilms in gram-negative bacteria. Here we show that the rice pathogen Burkholderia glumae BGR1 forms cellulase-sensitive pellicles in a bis-(3′-5′)-cyclic dimeric guanosine monophosphate (c-di-GMP)- and flagellum-dependent, but quorum sensing (QS)-independent, manner. Pellicle formation was more favorable at 28°C than at the optimum growth temperature (37°C), and was facilitated by constitutive expression of pelI, a diguanylate cyclase gene from B. glumae, or pleD, the GGDEF response regulator from Agrobacterium tumefaciens. Constitutive expression of pelI or pleD raised the levels of c-di-GMP, facilitated pellicle formation, and suppressed swarming motility in B. glumae. QS-defective mutants of B. glumae formed pellicles, while flagellum-defective mutants did not. Pellicles of B. glumae were sensitive to cellulase but not to proteinase K or DNase I. A gene cluster containing seven genes involved in bacterial cellulose biosynthesis, bcsD, bcsR, bcsQ, bcsA, bcsB, bcsZ, and bcsC, homologous to known genes involved in cellulose biosynthesis in other bacteria, was identified in B. glumae. Mutations in each gene abolished pellicle formation. These results revealed a positive correlation between cellulase-sensitive pellicles and putative cellulose biosynthetic genes. Pellicle-defective mutants did not colonize as successfully as the wild-type strain BGR1 in rice plants, which resulted in a significant reduction in virulence. Our findings show that cellulase-sensitive pellicles produced in a QS-independent manner play important roles in the interactions between rice plants and B. glumae.
Highlights
Bacterial biofilms are complex multicellular complexes embedded with self-producing extracellular materials such as polysaccharides, proteins, and nucleic acids (Donlan, 2002; Flemming et al, 2007)
To determine the major component of pellicles produced by B. glumae, we assessed the sensitivity of pellicles to cellulase, proteinase K, and DNase I
Our results revealed such cases where plant pathogenic bacteria interact with their hosts
Summary
Bacterial biofilms are complex multicellular complexes embedded with self-producing extracellular materials such as polysaccharides, proteins, and nucleic acids (Donlan, 2002; Flemming et al, 2007). Bacterial biofilms are generally developed on diverse solid surfaces, and biofilm formed at the air–liquid interface is called floating biofilm or pellicle (Armitano et al, 2014). Under unfavorable growth conditions or in certain ecological niches, bacterial cells form complex biofilm structures for their survival (Williams and Cannon, 1989; Kovács and Dragoš, 2019). Aerotactic bacterial cells are coagulated at the air–liquid interface by flagellum-mediated motility, switch their lifestyles to become sessile cells through bis-(3 -5 )-cyclic dimeric guanosine monophosphate (c-di-GMP)-mediated signal transduction systems (Römling et al, 2005, 2013; Römling and Amikam, 2006). Bacterial quorum sensing (QS) often plays critical roles in biofilm formation (Hentzer et al, 2004; De Kievit, 2009; Guttenplan and Kearns, 2013). Formation of pellicles provides fitness and survival advantages (Boles and Singh, 2008); the roles of cellulosic pellicles in the natural environment are not well understood, especially in interactions between plant pathogenic bacteria and their hosts
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