Signaling-mediated cross-talk modulates swarming and biofilm formation in a coral pathogen Serratia marcescens

Abstract

Interactions within microbial communities associated with marine holobionts contribute importantly to the health of these symbiotic organisms formed by invertebrates, dinoflagellates and bacteria. However, mechanisms that control invertebrate-associated microbiota are not yet fully understood. Hydrophobic compounds that were isolated from surfaces of asymptomatic corals inhibited biofilm formation by the white pox pathogen Serratia marcescens PDL100, indicating that signals capable of affecting the associated microbiota are produced in situ. However, neither the origin nor structures of these signals are currently known. A functional survey of bacteria recovered from coral mucus and from cultures of the dinoflagellate Symbiodinium spp. revealed that they could alter swarming and biofilm formation in S. marcescens. As swarming and biofilm formation are inversely regulated, the ability of some native a-proteobacteria to affect both behaviors suggests that the a-proteobacterial signal(s) target a global regulatory switch controlling the behaviors in the pathogen. Isolates of Marinobacter sp. inhibited both biofilm formation and swarming in S. marcescens PDL100, without affecting growth of the coral pathogen, indicative of the production of multiple inhibitors, likely targeting lower level regulatory genes or functions. A multi-species cocktail containing these strains inhibited progression of a disease caused by S. marcescens in a model polyp Aiptasia pallida. An a-proteobacterial isolate 44B9 had a similar effect. Even though B4% of native holobiont-associated bacteria produced compounds capable of triggering responses in well-characterized N-acyl homoserine lactone (AHL) biosensors, there was no strong correlation between the production of AHL-like signals and disruption of biofilms or swarming in S. marcescens.

Members of native coral microbiota inhibit glycosidases and thwart colonization of coral mucus by an opportunistic pathogen

“…To further characterize the potential coregulation of metabolic enzymes and motility, swarming motility of PDL100 was assayed with and without the commensals as in Alagely et al, 2011. When spotted onto AB swarm agar plate, PDL100 swarms (Figure 6a).…”

“…Coral-associated bacteria were isolated from mucus of A. palmata by dilution plating onto Glycerol Artificial Sea Water medium as in Ritchie, 2006. The identities of the marine isolates were confirmed by PCR-amplifying and sequencing fragments of their 16S rRNA genes as previously described (Alagely et al, 2011). Data are deposited in GenBank (Accession numbers JQ954975; JQ954976; JQ954977; JQ954978; JQ954979; JQ954980).…”

“…Five microliters of S. marcescens cultures were spotted onto AB swarm agar plate B2 cm from the disk containing commensals as described previously (Alagely et al, 2011). For swimming motility, 5 ml of each culture were stab inoculated into marine broth 0.3% agar plates 2 cm apart.…”

“…Coral commensals produce antibiotics, inhibitors of cell-to-cell communication, and currently unknown compounds capable of inhibiting swarming and biofilm formation (Ritchie, 2006;Nissimov et al, 2009;ShnitOrland and Kushmaro, 2009;Rypien et al, 2010;Tait et al, 2010;Alagely et al, 2011). When coral commensals capable of interfering with swarming and biofilm formation in a pathogen were precolonized onto a model polyp, they completely inhibited the progression of a disease caused by S. marcescens (Alagely et al, 2011). This is similar to the ability of the commensal microbiota of vertebrates to act as a barrier to colonization and infection by pathogens (Leatham et al, 2009).…”

Crustose coralline algal species host distinct bacterial assemblages on their surfaces

“…have been isolated from diverse marine environments and exhibit algicidal and antimicrobial activity (Skerratt et al, 2002). Members of this genus isolated from coral mucus reduced growth and biofilm formation of coral pathogens (Skerratt et al, 2002;Shnit-Orland and Kushmaro, 2009;Alagely et al, 2011). T. prototypum also had higher abundances than other CCA of an OTU (6908) in the order Rhodobacterales (2.26 ± 3.67%) that aligned weakly (88.6%) to species of Rhodobacteraceae and an OTU (8276) in the order Planctomycetales (1.93 ± 1.47%) that aligned weakly (87.7%) to Blastopirellula spp.…”