Competitive strategies differentiate closely related species of marine actinobacteria

Abstract

Although competition, niche partitioning, and spatial isolation have been used to describe the ecology and evolution of macro-organisms, it is less clear to what extent these principles account for the extraordinary levels of bacterial diversity observed in nature. Ecological interactions among bacteria are particularly challenging to address due to methodological limitations and uncertainties over how to recognize fundamental units of diversity and link them to the functional traits and evolutionary processes that led to their divergence. Here we show that two closely related marine actinomycete species can be differentiated based on competitive strategies. Using a direct challenge assay to investigate inhibitory interactions with members of the bacterial community, we observed a temporal difference in the onset of inhibition. The majority of inhibitory activity exhibited by Salinispora arenicola occurred early in its growth cycle and was linked to antibiotic production. In contrast, most inhibition by Salinispora tropica occurred later in the growth cycle and was more commonly linked to nutrient depletion or other sources. Comparative genomics support these differences, with S. arenicola containing nearly twice the number of secondary metabolite biosynthetic gene clusters as S. tropica, indicating a greater potential for secondary metabolite production. In contrast, S. tropica is enriched in gene clusters associated with the acquisition of growth-limiting nutrients such as iron. Coupled with differences in growth rates, the results reveal that S. arenicola uses interference competition at the expense of growth, whereas S. tropica preferentially employs a strategy of exploitation competition. The results support the ecological divergence of two co-occurring and closely related species of marine bacteria by providing evidence they have evolved fundamentally different strategies to compete in marine sediments.

Effects of Actinomycete Secondary Metabolites on Sediment Microbial Communities

“…While the ecological functions of bacterial sec- ondary metabolites remain poorly understood, even less is known about how these compounds may help structure bacterial communities. In this case, we selected the sediment-inhabiting marine actinomycete S. arenicola because it is a rich source of secondary metabolites and has been shown to employ interference competition as a competitive strategy (18). Although this species may be a rare member of the bacterial community, its mycelial growth form and ability to secrete biologically active secondary metabolites suggest that it could have a major impact on localized community structure, thereby contributing to sediment microbial heterogeneity.…”

“…The chemical repertoire of S. arenicola is large and includes the rifamycins (49), a group of ansamycin antibiotics with activity against Gram-positive bacteria (83). Rifamycin production has been shown to play a role in the competitive strategy of S. arenicola, which contrasts with the lack of production of any known antibiotics by the closely related species S. tropica (18). While many S. arenicola compounds have biological activity, their ecological functions remain unknown.…”

“…Ten bacterial strains were selected to test for sensitivity to S. arenicola culture extracts based on their relationships to taxa that were significantly affected in the mesocosm studies. Eight of these strains were isolated from tropical sediments as part of a previous study (18) and grown on A1 agar medium (10 g of starch, 4 g of yeast extract, 2 g of peptone, 22 g of Instant Ocean, 16 g of agar, 1 liter of deionized water). Myxococcus xanthus DK1622 (GenBank accession number CP000113) was kindly provided by Rolf Mueller (Saarland University) and grown on CTT agar (96), and Saprospira grandis (ATCC 23124) was purchased from the ATCC and grown on RL1 agar (2 g of yeast extract, 3 g of peptone, 0.5 g of KNO 3 All of the above strains were tested for sensitivity to extracts of S. arenicola strains CNY-679 and CNS-820 generated as previously described.…”

“…The structured nature of sediments provides opportunities for the development of microenvironments in which bacteria interact and compete using mechanisms such as the production of allelopathic secondary metabolites. While such competitive interactions have been addressed with marine bacteria (17,18), it remains unknown how competitive interactions structure sediment microbial communities.…”

“…Notably, these bacteria are a rich source of secondary metabolites (49), which have proven to be key phenotypic (50) and genotypic (45) features that differentiate the species. Secondary metabolism also distinguishes the competitive strategies employed by S. arenicola and S. tropica; in particular, the production of rifamycin antibiotics by S. arenicola contributes to its broad inhibitory capacity compared to that of the faster-growing S. tropica (18). With ϳ10% of the genome of S. arenicola devoted to secondary metabolism (45,51) and the potent bioactivity of its natural products, this species was an obvious choice to explore the effects of secondary metabolites on the sediment microbial community.…”