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.
Project description:Ecologists have long observed that consumers can maintain species diversity in communities of their prey. Many theories of how consumers mediate diversity invoke a tradeoff between species' competitive ability and their ability to withstand predation. Under this constraint, the best competitors are also most susceptible to consumers, preventing them from excluding other species. However, empirical evidence for competition-defense tradeoffs is limited and, as such, the mechanisms by which consumers regulate diversity remain uncertain. We performed a meta-analysis of 36 studies to evaluate the prevalence of the competition-defense tradeoff and its role in maintaining diversity in plant communities. We quantified species' responses to experimental resource addition and consumer removal as estimates of competitive ability and resistance to consumers, respectively. With this analysis, we found mixed empirical evidence for a competition-defense tradeoff; in fact, competitive ability tended to be weakly positively correlated with defense overall. However, when present, negative relationships between competitive ability and defense influenced species diversity in the manner predicted by theory. In the minority of communities for which a tradeoff was detected, species evenness was higher, and resource addition and consumer removal reduced diversity. Our analysis reframes the commonly held notion that consumers structure plant communities through a competition-defense tradeoff. Such a tradeoff can maintain diversity when present, but negative correlations between competitive ability and defense were less common than is often assumed. In this respect, this study supports an emerging theoretical paradigm in which predation interacts with competition to both enhance and reduce species diversity.
Project description:Several prominent hypotheses have been posed to explain the immense variability among plant species in defense against herbivores. A major concept in the evolutionary ecology of plant defenses is that tradeoffs of defense strategies are likely to generate and maintain species diversity. In particular, tradeoffs between constitutive and induced resistance and tradeoffs relating these strategies to growth and competitive ability have been predicted. We performed three independent experiments on 58 plant species from 15 different plant families to address these hypotheses in a phylogenetic framework. Because evolutionary tradeoffs may be altered by human-imposed artificial selection, we used 18 wild plant species and 40 cultivated garden-plant species. Across all 58 plant species, we demonstrate a tradeoff between constitutive and induced resistance, which was robust to accounting for phylogenetic history of the species. Moreover, the tradeoff was driven by wild species and was not evident for cultivated species. In addition, we demonstrate that more competitive species-but not fast growing ones-had lower constitutive but higher induced resistance. Thus, our multispecies experiments indicate that the competition-defense tradeoff holds for constitutive resistance and is complemented by a positive relationship of competitive ability with induced resistance. We conclude that the studied genetically determined tradeoffs are indeed likely to play an important role in shaping the high diversity observed among plant species in resistance against herbivores and in life history traits.
Project description:Plant species vary greatly in their responsiveness to nutritional soil mutualists, such as mycorrhizal fungi and rhizobia, and this responsiveness is associated with a trade-off in allocation to root structures for resource uptake. As a result, the outcome of plant competition can change with the density of mutualists, with microbe-responsive plant species having high competitive ability when mutualists are abundant and non-responsive plants having high competitive ability with low densities of mutualists. When responsive plant species also allow mutualists to grow to greater densities, changes in mutualist density can generate a positive feedback, reinforcing an initial advantage to either plant type. We study a model of mutualist-mediated competition to understand outcomes of plant-plant interactions within a patchy environment. We find that a microbe-responsive plant can exclude a non-responsive plant from some initial conditions, but it must do so across the landscape including in the microbe-free areas where it is a poorer competitor. Otherwise, the non-responsive plant will persist in both mutualist-free and mutualist-rich regions. We apply our general findings to two different biological scenarios: invasion of a non-responsive plant into an established microbe-responsive native population, and successional replacement of non-responders by microbe-responsive species. We find that resistance to invasion is greatest when seed dispersal by the native plant is modest and dispersal by the invader is greater. Nonetheless, a native plant that relies on microbial mutualists for competitive dominance may be particularly vulnerable to invasion because any disturbance that temporarily reduces its density or that of the mutualist creates a window for a non-responsive invader to establish dominance. We further find that the positive feedbacks from associations with beneficial soil microbes create resistance to successional turnover. Our theoretical results constitute an important first step toward developing a general understanding of the interplay between mutualism and competition in patchy landscapes, and generate qualitative predictions that may be tested in future empirical studies.
Project description:Background. The extent to which ectomycorrhizal fungi mediate primary production, carbon storage, and nutrient remineralization in terrestrial ecosystems depends upon fungal community composition. However, the factors that govern community composition at the root system scale are not well understood. Here, we explore a potential tradeoff between ectomycorrhizal fungal competitive ability and enzymatic function. Methods. We grew Pinus muricata (Bishop Pine) seedlings in association with ectomycorrhizal fungi from three different genera in a fully factorial experimental design. We measured seedling growth responses, ectomycorrhizal abundance, and the root tip activity of five different extracellular enzymes involved in the mobilization of carbon and phosphorus. Results. We found an inverse relationship between competitiveness, quantified based on relative colonization levels, and enzymatic activity. Specifically, Thelephora terrestris, the dominant fungus, had the lowest enzyme activity levels, while Suillus pungens, the least dominant fungus, had the highest. Discussion. Our results identify a tradeoff between competition and function in ectomycorrhizal fungi, perhaps mediated by the competing energetic demands associated with competitive interactions and enzymatic production. These data suggest that mechanisms such as active partner maintenance by host trees may be important to maintaining "high-quality" ectomycorrhizal fungal partners in natural systems.
Project description:Biological invasions can have various impacts on the diversity of important microbial mutualists such as mycorrhizal fungi, but few studies have tested whether the effects of invasions on mycorrhizal diversity are consistent across spatial gradients. Furthermore, few of these studies have taken place in tropical ecosystems that experience an inordinate rate of invasions into native habitats. Here, we examined the effects of plant invasions dominated by non-native tree species on the diversity of arbuscular mycorrhizal (AM) fungi in Hawaii. To test the hypothesis that invasions result in consistent changes in AM fungal diversity across spatial gradients relative to native forest habitats, we sampled soil in paired native and invaded sites from three watersheds and used amplicon sequencing to characterize AM fungal communities. Whether our analyses considered phylogenetic relatedness or not, we found that invasions consistently increased the richness of AM fungi. However, AM fungal species composition was not related to invasion status of the vegetation nor local environment, but stratified by watershed. Our results suggest that while invasions can lead to an overall increase in the diversity of microbial mutualists, the effects of plant host identity or geographic structuring potentially outweigh those of invasive species in determining the community membership of AM fungi. Thus, host specificity and spatial factors such as dispersal need to be taken into consideration when examining the effects of biological invasions on symbiotic microbes.
Project description:In this study, eight-month-old ectomycorrhizae of Tuber borchii with Corylus avellana were synthesized to explore the influence of T. borchii colonization on the soil properties and the microbial communities associated with C. avellana during the early symbiotic stage. The results showed that the bacterial richness and diversity in the ectomycorrhizae were significantly higher than those in the control roots, whereas the fungal diversity was not changed in response to T. borchii colonization. Tuber was the dominant taxon (82.97%) in ectomycorrhizae. Some pathogenic fungi, including Ilyonectria and Podospora, and other competitive mycorrhizal fungi, such as Hymenochaete, had significantly lower abundance in the T. borchii inoculation treatment. It was found that the ectomycorrhizae of C. avellana contained some more abundant bacterial genera (e.g., Rhizobium, Pedomicrobium, Ilumatobacter, Streptomyces, and Geobacillus) and fungal genera (e.g., Trechispora and Humicola) than the control roots. The properties of rhizosphere soils were also changed by T. borchii colonization, like available nitrogen, available phosphorus and exchangeable magnesium, which indicated a feedback effect of mycorrhizal synthesis on soil properties. Overall, this work highlighted the interactions between the symbionts and the microbes present in the host, which shed light on our understanding of the ecological functions of T. borchii and facilitate its commercial cultivation.
Project description:For many opportunistic pathogens, it is unclear why their virulence determinants and expression of pathogenic behavior have evolved when damage or death of their host offers no obvious selective advantage to microbial growth or survival. Many pathogens initiate interactions with their host on mucosal surfaces and must compete with other members of the microflora for the same niche. Here we explore whether competitive interactions between microbes promote the acquisition of virulence characteristics. During model murine nasal colonization, Haemophilus influenzae outcompetes another member of the local flora, Streptococcus pneumoniae, by recruiting neutrophils and stimulating the killing of complement-opsonized pneumococci. For S. pneumoniae, resistance to opsonophagocytic killing is determined by its polysaccharide capsule. Although there are many capsule types among different S. pneumoniae isolates that allow for efficient colonization, virulent pneumococci express capsules that confer resistance to opsonophagocytic clearance. Modeling of interspecies interaction predicts that these more virulent S. pneumoniae will prevail during competition with H. influenzae, even if production of a capsule is otherwise costly. Experimental colonization studies confirmed the increased survival of the more virulent S. pneumoniae type during competition. Our findings demonstrate that competition between microbes during their commensal state may underlie selection for characteristics that allow invasive disease.
Project description:Introduced species threaten native biodiversity, but whether exotic species can competitively displace native species remains contested. Building on theory that predicts multi-species coexistence based on a competition-colonisation tradeoff, we derive a mechanistic basis by which human-mediated species invasions could cause extinctions through competitive displacement. In contrast to past invasions, humans principally introduce modern invaders, repeatedly and in large quantities, and in ways that can facilitate release from enemies and competitors. Associated increases in exotic species' propagule rain, survival and competitive ability could enable some introduced species to overcome the tradeoffs that constrain all other species. Using evidence from metacommunity models, we show how species introductions could disrupt species coexistence, generating extinction debts, especially when combined with other forms of anthropogenic environmental change. Even though competing species have typically coexisted following past biogeographic migrations, the multiplicity and interactive impacts of today's threats could change some exotic species into agents of extinction.
Project description:Bacteria and fungi secrete antibiotics to suppress and kill other microbes, but can these compounds be agents of competition against macroorganisms? We explore how one competitive tactic, antibiotic production, can structure the composition and function of brown food webs. This aspect of warfare between microbes and invertebrates is particularly important today as antibiotics are introduced into ecosystems via anthropogenic activities, but the ecological implications of these introductions are largely unknown. We hypothesized that antimicrobial compounds act as agents of competition against invertebrate and microbial competitors. Using field-like mesocosms, we tested how antifungal and antibacterial compounds influence microbes, invertebrates, and decomposition in the brown food web. Both antibiotics changed prokaryotic microbial community composition, but only the antibacterial changed invertebrate composition. Antibacterials reduced the abundance of invertebrate detritivores by 34%. However, the addition of antimicrobials did not ramify up the food web as predator abundances were unaffected. Decomposition rates did not change. To test the mechanisms of antibiotic effects, we provided antibiotic-laden water to individual invertebrate detritivores in separate microcosm experiments. We found that the antibiotic compounds can directly harm invertebrate taxa, probably through a disruption of endosymbionts. Combined, our results show that antibiotic compounds could be an effective weapon for microbes to compete against both microbial and invertebrate competitors. In the context of human introductions, the detrimental effects of antibiotics on invertebrate communities indicates that the scope of this anthropogenic disturbance is much greater than previously expected.
Project description:Animal 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.The 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.