Isolation of an antimicrobial compound produced by bacteria associated with reef-building corals

Abstract

Bacterial communities associated with healthy corals produce antimicrobial compounds that inhibit the colonization and growth of invasive microbes and potential pathogens. To date, however, bacteria-derived antimicrobial molecules have not been identified in reef-building corals. Here, we report the isolation of an antimicrobial compound produced by Pseudovibrio sp. P12, a common and abundant coral-associated bacterium. This strain was capable of metabolizing dimethylsulfoniopropionate (DMSP), a sulfur molecule produced in high concentrations by reef-building corals and playing a role in structuring their bacterial communities. Bioassay-guided fractionation coupled with nuclear magnetic resonance (NMR) and mass spectrometry (MS), identified the antimicrobial as tropodithietic acid (TDA), a sulfur-containing compound likely derived from DMSP catabolism. TDA was produced in large quantities by Pseudovibrio sp., and prevented the growth of two previously identified coral pathogens, Vibrio coralliilyticus and V. owensii, at very low concentrations (0.5 μg/mL) in agar diffusion assays. Genome sequencing of Pseudovibrio sp. P12 identified gene homologs likely involved in the metabolism of DMSP and production of TDA. These results provide additional evidence for the integral role of DMSP in structuring coral-associated bacterial communities and underline the potential of these DMSP-metabolizing microbes to contribute to coral disease prevention.

Unexpected mixed-mode transmission and moderate genetic regulation ofSymbiodiniumcommunities in a brooding coral

“…The symbioses of Wolbachia and Spiroplasma bacteria among Drosophila and lepidopteran genera, for example, are highly specific and exclude other bacterial lineages through a dynamic and mature immune response, to the extent that specific Drosophila species host novel and specific Wolbachia and/or Spiroplasma strains [12,39]. Mechanisms of immunity that could be transmitted through inheritance of parental genes include components of both the innate and adaptive immune response, including some that have been implicated in shaping invertebrate symbiont communities, such as T-cells, Nod2, defensins, and antimicrobial peptides [as reviewed in 73,74]. These mechanisms have been documented during Symbiodinium establishment in corals [72,75,76] and observed in the Hydra/bacteria symbiosis [73,77].…”

Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria

“…Two different bacterial strains were added to the rinsed cultures and co-incubated for six hours: (i) Pseudovibrio sp. P12, a DMSP-degrading bacterium isolated from healthy corals (Raina et al, 2016), selected because of its worldwide distribution in coastal waters (Shieh et al, 2004) and its abundance in benthic invertebrate communities (Bondarev et al, 2013); and (ii) a control, Escherichia coli W (ATCC 9637), a widely studied and fully sequenced strain, able to grow in seawater and not capable of degrading DMSP. To precisely localise bacterial cells, both strains were pre-grown in a medium enriched in the rare stable isotope 15 N (in amino-acids and ammonium form).…”

“…We sequenced the genome of Pseudovibrio sp. P12, revealing that this bacterium harbours a complete DMSP cleavage pathway, including a DMSP acyl-CoA transferase (encoded by dddD ), a DMSP transporter ( dddT ) and the downstream catabolic enzymes ( dddB-C ) (Todd et al, 2007; Raina et al, 2016). Further analyses using NMR revealed that this DMSP degradation pathway was functional, enabling this strain to convert high concentrations of DMSP into DMS (Raina et al, 2016).…”

“…In addition, Pseudovibrio sp. P12 harbours homologues of genes involved in the demethylation pathway ( dmdA-B-C-D ), though these genes have a relatively low sequence identity (24%, 30%, 43% and 32%, respectively) (Raina et al, 2016) to the genes originally identified in Ruegeria pomeroyi DSS-3 (Reisch et al, 2011). …”

Disentangling causation: complex roles of coral‐associated microorganisms in disease

“…Symbiodinium also produce large amounts of dimethylsulfoniopropionate (DMSP) which is an integral organic sulfur source to various marine life and has been implicated in structuring coral‐associated bacterial communities (Frade et al ., ; Johnston et al ., ; Raina et al ., ). Raina and colleagues () identified an antimicrobial compound, tropodithietic acid (TDA), produced through bacterial mediated DMSP metabolism by the coral derived bacterial strain Pseudovibrio sp . P12, and suggested a potential role in modulating coral microbiomes and disease prevention.…”