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Competition-colonization tradeoffs structure fungal diversity.

ABSTRACT: Findings of immense microbial diversity are at odds with observed functional redundancy, as competitive exclusion should hinder coexistence. Tradeoffs between dispersal and competitive ability could resolve this contradiction, but the extent to which they influence microbial community assembly is unclear. Because fungi influence the biogeochemical cycles upon which life on earth depends, understanding the mechanisms that maintain the richness of their communities is critically important. Here, we focus on ectomycorrhizal fungi, which are microbial plant mutualists that significantly affect global carbon dynamics and the ecology of host plants. Synthesizing theory with a decade of empirical research at our study site, we show that competition-colonization tradeoffs structure diversity in situ and that models calibrated only with empirically derived competition-colonization tradeoffs can accurately predict species-area relationships in this group of key eukaryotic microbes. These findings provide evidence that competition-colonization tradeoffs can sustain the landscape-scale diversity of microbes that compete for a single limiting resource.

SUBMITTER: Smith GR

PROVIDER: S-EPMC6018791 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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Competition-colonization tradeoffs structure fungal diversity.

Smith Gabriel R GR Steidinger Brian S BS Bruns Thomas D TD Peay Kabir G KG

The ISME journal 20180228 7

Findings of immense microbial diversity are at odds with observed functional redundancy, as competitive exclusion should hinder coexistence. Tradeoffs between dispersal and competitive ability could resolve this contradiction, but the extent to which they influence microbial community assembly is unclear. Because fungi influence the biogeochemical cycles upon which life on earth depends, understanding the mechanisms that maintain the richness of their communities is critically important. Here, w ...[more]

PMID: 29491493

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Project description:UnlabelledAnimal development and physiology depend on beneficial interactions with microbial symbionts. In many cases, the microbial symbionts are horizontally transmitted among hosts, thereby making the acquisition of these microbes from the environment an important event within the life history of each host. The light organ symbiosis established between the Hawaiian squid Euprymna scolopes and the bioluminescent bacterium Vibrio fischeri is a model system for examining how hosts acquire horizontally transmitted microbial symbionts. Recent studies have revealed that the light organ of wild-caught E. scolopes squid contains polyclonal populations of V. fischeri bacteria; however, the function and development of such strain diversity in the symbiosis are unknown. Here, we report our phenotypic and phylogenetic characterizations of FQ-A001, which is a V. fischeri strain isolated directly from the light organ of an E. scolopes individual. Relative to the type strain ES114, FQ-A001 exhibits similar growth in rich medium but displays increased bioluminescence and decreased motility in soft agar. FQ-A001 outcompetes ES114 in colonizing the crypt spaces of the light organs. Remarkably, we find that animals cocolonized with FQ-A001 and ES114 harbor singly colonized crypts, in contrast to the cocolonized crypts observed from competition experiments involving single genotypes. The results with our two-strain system suggest that strain diversity within the squid light organ is a consequence of diversity in the single-strain colonization of individual crypt spaces.ImportanceThe developmental programs and overall physiologies of most animals depend on diverse microbial symbionts that are acquired from the environment. However, the basic principles underlying how microbes colonize their hosts remain poorly understood. Here, we report our findings of bacterial strain competition within the coevolved animal-microbe symbiosis composed of the Hawaiian squid and bioluminescent bacterium Vibrio fischeri Using fluorescent proteins to differentially label two distinct V. fischeri strains, we find that the strains are unable to coexist in the same niche within the host. Our results suggest that strain competition for distinct colonization sites dictates the strain diversity associated with the host. Our study provides a platform for studying how strain diversity develops within a host.

Project description:BACKGROUND: Ophiocordyceps sinensis (syn. Cordyceps sinensis), which is a parasite of caterpillars and is endemic to alpine regions on the Tibetan Plateau, is one of the most valuable medicinal fungi in the world. "Natural O. sinensis specimens" harbor various other fungi. Several of these other fungi that have been isolated from natural O. sinensis specimens have similar chemical components and/or pharmaceutical effects as O. sinensis. Nevertheless, the mycobiota of natural O. sinensis specimens has not been investigated in detail. METHODOLOGY/PRINCIPAL FINDINGS: Based on the technique of PCR-single-strand conformation polymorphism (PCR-SSCP), the mycobiota of three different sections (stromata, sclerotia, and mycelial cortices) from natural O. sinensis specimens were investigated using both culture-dependent and -independent methods. For the culture-dependent method, 572 fungal strains were isolated, and 92 putative operational taxonomic units (OTUs) were identified from 226 sequenced strains with the threshold of 97%. For the culture-independent method, 490 fungal clones were identified from about 3000 clones of ITS fragments from the whole-community DNA; based on PCR-SSCP analyses, 266 of these clones were selected to be sequenced, and 118 putative OTUs were detected. The overwhelming majority of isolates/clones and OTUs were detected from mycelial cortices; only a few were detected from stromata and sclerotia. The most common OTUs detected with both methods belonged to Ascomycota; however, only 13 OTUs were detected simultaneously by both methods. Potential novel lineages were detected by each of the two methods. CONCLUSIONS/SIGNIFICANCE: A great number of fungal species present in the mycobiota of naturally-occurring O. sinensis specimens were detected, and many of them may represent undescribed lineages. That only a few of the same OTUs were detected by both methods indicated that different methods should be used. This study increased our understanding about the fungal community structure of this valuable medicinal herb.

Dataset Information

Competition-colonization tradeoffs structure fungal diversity.

Publications

Competition-colonization tradeoffs structure fungal diversity.

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