Competitive exclusion as a mode of action of a novel Bacillus cereus aquaculture biological agent

Abstract

Aims: To determine the contribution of potential modes of action of a Bacillus cereus aquaculture biological control agent in inhibition of the fish pathogen, Aeromonas hydrophila. Methods and Results: When B. cereus was tested in plate well inhibition studies, no production of antimicrobial compounds was detected. Bacillus cereus had a high growth rate (0·96 h−1), whereas Aer. hydrophila concentration decreased by c. 70% in co‐culture experiments. In nutrient limitation studies, B. cereus had a significantly higher growth rate when cultured under glucose (P < 0·05) and iron (P < 0·01) limitation in comparison with Aer. hydrophila. Bacillus cereus glucose (0·30 g l−1 h−1) and iron (0·60 mg l−1 h−1) uptake rates were also significantly higher (P < 0·01) than the Aer. hydrophila glucose (0·14 g l−1 h−1) and iron (0·43 mg l−1 h−1) uptake rates. Iron uptake was facilitated by siderophore production shown in time profile studies where relative siderophore production was c. 60% through the late exponential and sporulation phases. Conclusions: Competitive exclusion by higher growth rate, competition for organic carbon and iron, facilitated by siderophore production, could be identified as mechanisms of pathogen growth inhibition by B. cereus. Significance and Impact of the Study: This study is the first elucidation of the mechanism of action of our novel B. cereus biological agent in growth attenuation of pathogenic Aer. hydrophila. This study enhances the application knowledge and attractiveness for adoption of B. cereus NRRL 100132 for exploitation in aquaculture.

Selection and probiotic characterization of exoenzyme-producing bacteria isolated from the gut of Catla catla (Actinopterygii: Cypriniformes: Cyprinidae)

“…Nonetheless, it could be hypothesized from the present investigation that the extracellular enzyme-producing bacteria colonizing within the GI tract of Catla catla might offer protection against the pathogenic Aeromonas strains. Although, the mechanism of inhibition was not characterized here, preceding studies suggested that the growth of pathogens (e.g., A. hydrophila) might be inhibited by competitive exclusion, competition for essential nutrients (e.g., glucose and iron) and siderophore production (Lalloo et al 2010). The method used in the presently reported study to assay the antagonistic effect of the putative probiotics (agar-overlay/double-layer) demonstrates the infl uence of diffusing antimicrobial products on growth of the pathogenic bacteria.…”

“…In comparison, pathogen inhibitory potential of the bacilli has been rarely indicated. B. subtilis SG4 isolated from the gut of mrigal, C. mrigala (see Ghosh et al 2007), B. methylotrophicus isolated from channel catfi sh intestine (Ran et al 2012), and B. cereus and B. circulans isolated from the gut of some other fi sh species (Lalloo et al 2010, Geraylou et al 2014) were reported to be antagonistic against different strains of A. hydrophila. In addition, enzyme-producing B. thuringiensis isolated from the GI tract of the Atlantic salmon, Salmo salar Linnaeus, 1758, was shown to inhibit A. salmonicida subsp.…”

Siderophores in environmental research: roles and applications

“…strain NM 12 produces siderophores with a wide antibacterial spectrum that inhibited the growth of 62.5% of 363 intestinal bacteria identified from several coastal fishes (Li and Chi, 2004). In addition, siderophores produced by Bacillus cereus has also been found to inhibit the growth of the fish pathogen Aeromonas hydrophila (Lalloo et al, 2010). Recently it was found that several siderophore-producing bacteria isolated from the intestinal tracts of fishes inhibit fish pathogens such as Aliivibrio logei, Vibrio ichthyoenteri, V. anguillarum, Vibrio splendidus and A. salmonicida (Sugita et al, 2012).…”

Application of Probiotics in Shrimp Aquaculture: Importance, Mechanisms of Action, and Methods of Administration

“…It is well known that the gastrointestinal microbiota of aquatic animals can be modified, for example, by ingestion of other microorganism; therefore, microbial manipulation constitutes a viable tool to reduce or eliminate the incidence of opportunistic pathogen (Balcazar, 2002). The direct effect, such as inhibiting the growth of other microorganisms, might be the main action that can occur in cultured systems (Kesarcodi-Watson et al, 2008;Jiang et al, 2013;Giri et al, 2013), and studies have illustrated that indigenous microorganisms have great potential because of the higher probability of competitive exclusion due to adaptation to the same ecological niche (Lalloo et al, 2010). Adhesion and colonization on the mucosal surfaces are possible protective mechanisms against pathogens through competition for binding sites and nutrients (Salyers and White, 2002).…”