Degradation of gallic acid and hydrolysable polyphenols is constitutively activated in the freshwater plant-associated bacterium Matsuebacter sp. FB25

Abstract

Hydrolysable polyphenols are present in Myriophyllum spicatum L. at high concentrations of up to 25% of dry matter and are also excreted. Bacteria associated with the submerged macrophyte M. spicatum isolated from the surrounding water column and epiphytic biofilm were tested for their ability to degrade polyphenols. Several bacterial isolates were capable of growing with tannic acid as the sole carbon and energy source, among them Matsuebacter sp. FB25, Agrobacterium vitis EB26 and Pseudomonas sp. FB22. Cell suspensions of Matsuebacter sp. precultured on succinate were capable of degrading gallic acid, while those of A. vitis were not, indicating the constitutive presence of gallate-degrading enzymes in the former. When cells were precultured on gallic or tannic acid, cell suspensions of both strains exhibited an enhanced degradation rate of gallic acid. M. spicatum-derived hydrolysable polyphenols, which are comparable in structure to tannic acid, resulted in the same enhanced degradation rate of gallic acid or tellimagrandin II, the major M. spicatum polyphenol, by cell suspensions of Matsuebacter sp. FB25. The presence of polyphenoldegrading bacteria in the vicinity of M. spicatum explains the observed fast disappearance of tellimagrandin II and other hydrolysable polyphenols after excretion and has implications for allelochemical interference with competitors, herbivores and potential pathogenic microorganisms. The presence of Matsuebacter sp. and other polyphenol-degrading strains in such environments suggests a sufficiently strong effect of M. spicatum exudates to bring about selection in favour of highly specialised bacteria.KEY WORDS: Hydrolysable polyphenol · Submerged macrophyte · Allelochemistry · Biofilm · Betaproteobacteria · Burkholderiales · Myriophyllum spicatum · TanninResale or republication not permitted without written consent of the publisher

Allelopathic effects of submerged macrophytes on phytoplankton

“…Müller et al (2007) were the first to show that distinct bacterial groups isolated from the biofilm and the surrounding water column of the allelopathically active submerged macrophyte M. spicatum are able to degrade polyphenolic allelochemicals. This was surprising as polyphenols are known for their anti-bacterial properties (Walenciak et al, 2002), and polyphenol degrading bacteria were only known from anaerobic environments (Mahadevan and Muthukumar, 1980;Schink et al, 2000).…”

“…Until now however, most studies on allelopathic effects of macrophytes on algae were carried out either with axenic or xenic algal cultures with an undefined bacterial community. Both treatments do not accommodate the possible effect of the bacterial community which may metabolize allelochemicals (Müller et al, 2007), transform them biochemically (Scalbert, 1991), build mechanical barriers such as extracellular polysaccharides (Decho, 1990) or otherwise interact with the phytoplankton species via symbiosis, commensalism or antagonism (Cole, 1982;Grossart, 1999).…”

Can allelopathically active submerged macrophytes stabilise clear-water states in shallow lakes?

“…Herbivory on M. spicatum apical meristems, which contain the highest concentrations of allelopathically active hydrolysable polyphenols, should severely hamper the negative impact on phytoplankton (Choi, Bareiss, Walenciak, & Gross, 2002). The same polyphenols exert some antimicrobial activity (Walenciak, Zwisler, & Gross, 2002), although other microbes are capable of their degradation (Mu¨ller, Hempel, Philipp, & Gross, 2007). Light and UV light stress or nutrient limitations (see below) also affect secondary metabolites, among them allelopathically active polyphenols in M. spicatum (Gross, 2003b).…”

“…Pre-treatment of the natural bacterial community with TA resulted in a change of the natural bacterial community towards potentially TA-resistant or metabolising bacteria (Bauer et al, unpublished). Specific polyphenol-degrading bacteria, as recently isolated from M. spicatum, may have a strong impact on the inhibitory effect of the macrophyte exudates (Mu¨ller et al, 2007).…”

Gut pH, redox conditions and oxygen levels in an aquatic caterpillar: Potential effects on the fate of ingested tannins

“…/j.jinsphys.2007 or M. spicatum are inhibited by TII and other polyphenols in vitro . Other bacteria found in the biofilm on M. spicatum or the surrounding water can degrade such polyphenols (Mu¨ller et al, 2007).…”