Abstract
The soil bacterium Bacillus subtilis is often found in association with plants in the rhizosphere. Previously, plant polysaccharides have been shown to stimulate formation of root-associated multicellular communities, or biofilms, in this bacterium, yet the underlying mechanism is not fully understood. A five-gene gan operon (ganSPQAB) in B. subtilis has recently been shown to be involved in utilization of the plant-derived polysaccharide galactan. Despite these findings, molecular details about the regulation of the operon and the role of the operon in biofilm formation remain elusive. In this study, we performed comprehensive genetic analyses on the regulation of the gan operon. We show that this operon is regulated both by a LacI-like transcription repressor (GanR), which directly binds to pairs of inverted DNA repeats in the promoter region of the operon, and by the catabolite control protein A (CcpA). Derepression can be triggered by the presence of the inducer β-1,4-galactobiose, a hydrolysis product of galactan, or in situ when B. subtilis cells are associated with plant roots. In addition to the transcriptional regulation, the encoded ß-galactosidase GanA (by ganA), which hydrolyzes ß-1,4-galactobiose into galactose, is inhibited at the enzymatic level by the catalytic product galactose. Thus, the galactan utilization pathway is under complex regulation involving both positive and negative feedback mechanisms in B. subtilis. We discuss about the biological significance of such complex regulation as well as a hypothesis of biofilm induction by galactan via multiple mechanisms.
Highlights
Bacillus subtilis is a Gram-positive, soil-dwelling, spore-forming bacterium, commonly found in the rhizosphere and often in association with plant roots [1, 2]
In our previous study [20], we presented evidence that the gan operon is part of the pathway involved in utilization of plant polysaccharide galactan; growth of the B. subtilis mutant (ΔganSPQAB) was partially impaired when cells were grown in a minimal medium with galactan as the sole carbon source [20]
We further found that addition of galactan (0.5%, w/v) in lysogenic broth (LB), a less favorable medium for biofilm formation, promoted pellicle biofilm formation in B. subtilis NCIB3610
Summary
Bacillus subtilis is a Gram-positive, soil-dwelling, spore-forming bacterium, commonly found in the rhizosphere and often in association with plant roots [1, 2]. Regulation of the gan operon in B. subtilis plant polysaccharides and are of great interest in agriculture, industry, and biotechnology [4, 5]. Those secreted enzymes, and the corresponding gene clusters and pathways for plant polysaccharide utilization, have been investigated in B. subtilis, and are proposed to play important roles in helping B. subtilis cells acquire carbon sources from the environment and in promoting fitness and survival of the bacterium in the rhizosphere, though the exact mechanisms are largely unknown [3,4,5,6]. The role of plant-released signals and the importance of plant-released nutrients on B. subtilis biofilm formation in situ are much less known
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