Specialized Metabolite-Mediated Predation Defense in the Marine Actinobacterium Salinispora

• Published in: Applied and environmental microbiology Vol. 88; no. 1; p. e0117621
• Main Authors: Tuttle, Robert N., Rouse, Greg W., Castro-Falcón, Gabriel, Hughes, Chambers C., Jensen, Paul R.
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 11.01.2022
• Subjects: Actinobacteria; Animals; Aquatic habitats; Bacteria; Biological activity; Caenorhabditis elegans; Community structure; Cytotoxicity; Defense; E coli; Ecological function; Ecosystem; Environmental Microbiology; Eukaryotes; Habitat preferences; Marine sediments; Metabolites; Microbial Ecology; Micromonosporaceae; Microorganisms; Natural products; Nematodes; Ophryotrocha; Predation; Predators; Predatory Behavior; Sediments; Species; Spotlight Selection; Worms; chemical defense; Salinispora; predation
• ISSN: 0099-2240; 1098-5336; 1098-5336
• DOI: 10.1128/AEM.01176-21

Bacteria inhabiting marine sediments are subject to predation by bacterivorous eukaryotes. Here, we test the hypothesis that sediment-derived bacteria in the genus Salinispora produce biologically active natural products that function as a defense against predation. The obligate marine actinobacterial genus Salinispora has become a model organism for natural product discovery, yet little is known about the ecological functions of the compounds produced by this taxon. The aims of this study were to assess the effects of live cultures and culture extracts from two Salinispora species on invertebrate predators. In choice-based feeding experiments using the bacterivorous nematode Caenorhabditis elegans , live cultures of both Salinispora species were less preferred than Escherichia coli . When given a choice between the two species, C. elegans preferred S. areniolca over S. tropica . Culture extracts from S. tropica deterred C. elegans , while those from S. arenicola did not, suggesting that compounds produced by S. tropica account for the feeding deterrence. Bioactivity-guided isolation linked compounds in the lomaiviticin series to the deterrent activity. Additional assays using the marine polychaete Ophryotrocha siberti and marine nematodes further support the deterrent activity of S. tropica against potential predators. These results provide evidence that Salinispora natural products function as a defense against predation and that the strategies of predation defense differ between closely related species. IMPORTANCE Bacteria inhabiting marine sediments are subject to predation by bacterivorous eukaryotes. Here, we test the hypothesis that sediment-derived bacteria in the genus Salinispora produce biologically active natural products that function as a defense against predation. The results reveal that cultures and culture extracts of S. tropica deter feeding by Caenorhabditis elegans and negatively affect the habitat preference of a marine annelid ( Ophryotrocha siberti ). These activities were linked to the lomaiviticins, a series of cytotoxic compounds produced by S. tropica . Microbial natural products that function as a defense against predation represent a poorly understood trait that can influence community structure in marine sediments.