Abstract
Komagataeibacter (formerly Gluconacetobacter) xylinus ATCC 53582 is a plant-associated model organism for bacterial cellulose (BC) biosynthesis. This bacterium inhabits the carposphere where it interacts with fruit through the bi-directional transfer of phytohormones. The majority of research regarding K. xylinus has been focused on identifying and characterizing structural and regulatory factors that control BC biosynthesis, but its ecophysiology has been generally overlooked. Ethylene is a phytohormone that regulates plant development in a variety of ways, but is most commonly known for its positive role on fruit ripening. In this study, we utilized ethephon (2-chloroethylphosphonic acid) to produce in situ ethylene to investigate the effects of this phytohormone on BC production and the expression of genes known to be involved in K. xylinus BC biosynthesis (bcsA, bcsB, bcsC, bcsD, cmcAx, ccpAx and bglAx). Using pellicle assays and reverse transcription quantitative polymerase chain reaction (RT-qPCR), we demonstrate that ethephon-derived ethylene enhances BC directly in K. xylinus by up-regulating the expression of bcsA and bcsB, and indirectly though the up-regulation of cmcAx, ccpAx, and bglAx. We confirm that IAA directly decreases BC biosynthesis by showing that IAA down-regulates bcsA expression. Similarly, we confirm that ABA indirectly influences BC biosynthesis by showing it does not affect the expression of bcs operon genes. In addition, we are the first to report the ethylene and indole-3-acetic acid (IAA) induced differential expression of genes within the bacterial cellulose synthesis (bcs) operon. Using bioinformatics we have identified a novel phytohormone-regulated CRP/FNRKx transcription factor and provide evidence that it influences BC biosynthesis in K. xylinus. Lastly, utilizing current and previous data, we propose a model for the phytohormone-mediated fruit-bacteria interactions that K. xylinus experiences in nature.
Highlights
Komagataeibacter xylinus ATCC 53582 is an acetic acid bacterium (Yamada et al, 2012; Mamlouk and Gullo, 2013) studied for its ability to synthesize and secrete large quantities of crystalline cellulose at the air−liquid interface of static cultures (Schramm and Hestrin, 1954)
Since this study focused on a small subset of genes, it is likely that abscisic acid (ABA) regulates a yet to be identified gene whose protein product counteracts the down-regulation of crp/fnrkx underscoring the complexity of the regulatory pathway involved in controlling Bacterial cellulose (BC) synthesis
We have demonstrated that ethylene produced through the in situ decomposition of ethephon can be used to study the effects of this hormone on bacteria
Summary
Komagataeibacter (formerly Gluconacetobacter) xylinus ATCC 53582 is an acetic acid bacterium (Yamada et al, 2012; Mamlouk and Gullo, 2013) studied for its ability to synthesize and secrete large quantities of crystalline cellulose at the air−liquid interface of static cultures (Schramm and Hestrin, 1954). Komagataeibacter xylinus and related species can be isolated from fruit (Park et al, 2003; Dellaglio et al, 2005; Jahan et al, 2012; Neera et al, 2015) and spoiled wine (Bartowsky and Henschke, 2008). The BC matrix provides protection from environmental stresses and provides a competitive advantage over other microorganisms (Williams and Cannon, 1989) This phenomenon is observed with Enterobacter amnigenus GH1, which synthesizes BC to adhere to fruits and abiotic materials (Kim et al, 2006; Hungund and Gupta, 2010). The role of BC in facilitating the diverse environmental interactions of various biofilm-producing bacteria has recently been reviewed (Augimeri et al, 2015)
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