Coral-associated bacteria, quorum sensing disrupters, and the regulation of biofouling

Abstract

Marine biofouling, the settlement of microorganisms and macroorganisms on structures submerged in seawater, although economically detrimental, is a successful strategy for survival in hostile environments, where coordinated bacterial communities establish biofilms via the regulation of quorum sensing (QS) communication systems. The inhibition of QS activity among bacteria isolated from different coral species was investigated to gain further insight into its potency in the attenuation, or even the prevention, of undesirable biofouling on marine organisms. It is hypothesized that coral mucus/microorganism interactions are competitive, suggesting that the dominant communities secrete QS disruptive compounds. One hundred and twenty bacterial isolates were collected from healthy coral species and screened for their ability to inhibit QS using three bioreporter strains. Approximately 12, 11, and 24% of the isolates exhibited anti-QS activity against Escherichia coli pSB1075, Chromobacterium violaceum CV026, and Agrobacterium tumefaciens KYC55 indicator strains, respectively. Isolates with positive activity against the bioluminescent monitor strains were scanned via a cytotoxic/genotoxic, E. coli TV1061 and DPD2794 antimicrobial panel. Isolates detected by C. violaceum CV026 and A. tumefaciens KYC55 reporter strains were tested for their ability to inhibit the growth of these reporter strains, which were found to be unaffected. Tests of the Favia sp. coral isolate Fav 2-50-7 (>98% similarity to Vibrio harveyi) for its ability to attenuate the formation of biofilm showed extensive inhibitory activity against biofilms of Pseudomonas aeruginosa and Acinetobacter baumannii. To ascertain the stability and general structure of the active compound, cell-free culture supernatants exposed to an increasing temperature gradient or to digestion by proteinase K, were shown to maintain potent QS attenuation and the ability to inhibit the growth of biofilms. Mass spectrometry confirmed the presence of a low molecular mass compound. The anti-QS strategy exemplified in the coral mucus is a model with potentially wide applications, including countering the ecological threat posed by biofilms. Manipulating synchronized bacterial behavior by detecting new QS inhibitors will facilitate the discovery of new antifouling compounds.

Microbiome shifts and the inhibition of quorum sensing by Black Band Disease cyanobacteria

“…Vibrios have previously been postulated to have a role in BBD (Barneah et al, 2007;Arotsker et al, 2009), although their contribution to the initiation and progression of the disease has yet to be characterized. Although vibrios were detected at moderately low levels in both healthy coral mucus and in the black band, vibrios are readily cultivable from both sample types and have QS activity through both the AHL-based autoinducer 1 system and the furanosyl borate diester-based autoinducer 2 system (Tait et al, 2010;Alagely et al, 2011a;Golberg et al, 2011Golberg et al, , 2013Zimmer et al, 2014). In addition to AHLs and AI-2, vibrios also produce hydroxyketone CAI-1 signals (Henke and Bassler, 2004;Ng et al, 2011;Wei et al, 2012), and with this study we demonstrate that coral vibrios also produce CAI-1-like activities.…”

Antibiofilm activity substances derived from coral symbiotic bacterial extract inhibit biofouling by the model strainPseudomonas aeruginosaPAO1

“…Because this bacterial biofilm formation is, in part, controlled by QS, various QSI strategies have been harnessed from marine microorganisms as compounds which could be used to interfere with bacterial QS, and thus represent novel forms of antifouling agents (Qian and Dahms, 2008; Dobretsov et al ., 2011). Among the array of marine niches, screening for antifouling compounds from coral symbiotic microbes is of particular interest because of their high biodiversity and rich secondary metabolism (Mohamed et al ., 2008; Fusetani, 2011; Karina et al ., 2013). In our present study, we found that 15% of coral‐associated bacteria exhibited inhibition activity against C. violaceum 12472.…”

“…In our present study, we found that 15% of coral‐associated bacteria exhibited inhibition activity against C. violaceum 12472. Previous studies reported that approximately 11–24% of the coral‐associated bacteria sampled were capable of QS inhibition activity against E. coli pSB1075, C. violaceum CV026 and A. tumefaciens KYC55 indicator strains (Romero et al ., 2011; Karina et al ., 2013). Our results are in line with these proportions and further suggest that coral ecosystems represent an ideal reservoir from which to develop QSI products.…”

“…Therefore, using QS inhibitors or QSI compounds that degrade signalling molecules to mitigate biofilm fouling represents a significant breakthrough (Dobretsov, 2009). Since then, several studies have demonstrated that QSI compounds are capable of reducing the formation of biofilm and further inhibit the development of biofouling (Cushnie and Lamb, 2011; Dobretsov et al ., 2011; Karina et al ., 2013). Some antifouling substances have recently been identified in microbes and plants (and even animals); these are peptide compounds, such as quorum‐quenching enzyme and small‐molecule compounds (Huang et al ., 2016; Bzdrenga et al ., 2017).…”

“…Compared with the planktonic environment, coral ecosystems have a much higher biodiversity and represent a potential source from which to isolate QS inhibitors. Indeed, several studies have described the QSI or antibiofilm potential of several natural compounds originating from coral, including the soft coral Antillogorgia elisabethae , the black coral Antipathes dichotoma , the octocoral Eunicea knighti and the cave coral Acropora millepora (Tello et al ., 2012; Karina et al ., 2013; Diana et al ., 2016). The wide existence of QSI bacteria in coral environments invites us to explore the feasibility of QSI‐based biofouling control methods.…”