Dataset Information

Biotic Interactions Shape the Ecological Distributions of Staphylococcus Species.

ABSTRACT: Many metagenomic sequencing studies have observed the presence of closely related bacterial species or genotypes in the same microbiome. Previous attempts to explain these patterns of microdiversity have focused on the abiotic environment, but few have considered how biotic interactions could drive patterns of microbiome diversity. We dissected the patterns, processes, and mechanisms shaping the ecological distributions of three closely related Staphylococcus species in cheese rind biofilms. Paradoxically, the most abundant species (S. equorum) is the slowest colonizer and weakest competitor based on growth and competition assays in the laboratory. Through in vitro community reconstructions, we determined that biotic interactions with neighboring fungi help resolve this paradox. Species-specific stimulation of the poor competitor by fungi of the genus Scopulariopsis allows S. equorum to dominate communities in vitro as it does in situ Results of comparative genomic and transcriptomic experiments indicate that iron utilization pathways, including a homolog of the S. aureus staphyloferrin B siderophore operon pathway, are potential molecular mechanisms underlying Staphylococcus-Scopulariopsis interactions. Our integrated approach demonstrates that fungi can structure the ecological distributions of closely related bacterial species, and the data highlight the importance of bacterium-fungus interactions in attempts to design and manipulate microbiomes.

Importance

Decades of culture-based studies and more recent metagenomic studies have demonstrated that bacterial species in agriculture, medicine, industry, and nature are unevenly distributed across time and space. The ecological processes and molecular mechanisms that shape these distributions are not well understood because it is challenging to connect in situ patterns of diversity with mechanistic in vitro studies in the laboratory. Using tractable cheese rind biofilms and a focus on coagulase-negative staphylococcus (CNS) species, we demonstrate that fungi can mediate the ecological distributions of closely related bacterial species. One of the Staphylococcus species studied, S. saprophyticus, is a common cause of urinary tract infections. By identifying processes that control the abundance of undesirable CNS species, cheese producers will have more precise control on the safety and quality of their products. More generally, Staphylococcus species frequently co-occur with fungi in mammalian microbiomes, and similar bacterium-fungus interactions may structure bacterial diversity in these systems.

SUBMITTER: Kastman EK

PROVIDER: S-EPMC5082897 | biostudies-literature | 2016 Oct

REPOSITORIES: biostudies-literature

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Biotic Interactions Shape the Ecological Distributions of Staphylococcus Species.

Kastman Erik K EK Kamelamela Noelani N Norville Josh W JW Cosetta Casey M CM Dutton Rachel J RJ Wolfe Benjamin E BE

mBio 20161018 5

Many metagenomic sequencing studies have observed the presence of closely related bacterial species or genotypes in the same microbiome. Previous attempts to explain these patterns of microdiversity have focused on the abiotic environment, but few have considered how biotic interactions could drive patterns of microbiome diversity. We dissected the patterns, processes, and mechanisms shaping the ecological distributions of three closely related Staphylococcus species in cheese rind biofilms. Par ...[more]

PMID: 27795388

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Project description:Abiotic factors are usually considered key drivers of species distribution at macro scales, while biotic interactions are mostly used at local scales. A few studies have explored the role of biotic interactions at macro scales, but all considered a limited number of species and obligate interactions. We examine the role of biotic interactions in large-scale SDMs by testing two main hypotheses: (1) biotic factors in SDMs can have an important role at continental scale; (2) the inclusion of biotic factors in large-scale SDMs is important also for generalist species. We used a maximum entropy algorithm to model the distribution of 177 bat species in Africa calibrating two SDMs for each species: one considering only abiotic variables (noBIO-SDMs) and the other (BIO-SDMs) including also biotic variables (trophic resource richness). We focused the interpretation of our results on variable importance and response curves. For each species, we also compared the potential distribution measuring the percentage of change between the two models in each pixel of the study area. All models gave AUC >0.7, with values on average higher in BIO-SDMs compared to noBIO-SDMs. Trophic resources showed an importance overall higher level than all abiotic predictors in most of the species (~68%), including generalist species. Response curves were highly interpretable in all models, confirming the ecological reliability of our models. Model comparison between the two models showed a change in potential distribution for more than 80% of the species, particularly in tropical forests and shrublands. Our results highlight the importance of considering biotic interactions in SDMs at macro scales. We demonstrated that a generic biotic proxy can be important for modeling species distribution when species-specific data are not available, but we envision that a multi-scale analysis combined with a better knowledge of the species might provide a better understanding of the role of biotic interactions.

Project description:BackgroundUnderstanding the factors that shape the distribution of tropical tree species at large scales is a central issue in ecology, conservation and forest management. The aims of this study were to (i) assess the importance of environmental factors relative to historical factors for tree species distributions in the semi-evergreen forests of the northern Congo basin; and to (ii) identify potential mechanisms explaining distribution patterns through a trait-based approach.Methodology/principal findingsWe analyzed the distribution patterns of 31 common tree species in an area of more than 700,000 km(2) spanning the borders of Cameroon, the Central African Republic, and the Republic of Congo using forest inventory data from 56,445 0.5-ha plots. Spatial variation of environmental (climate, topography and geology) and historical factors (human disturbance) were quantified from maps and satellite records. Four key functional traits (leaf phenology, shade tolerance, wood density, and maximum growth rate) were extracted from the literature. The geological substrate was of major importance for the distribution of the focal species, while climate and past human disturbances had a significant but lesser impact. Species distribution patterns were significantly related to functional traits. Species associated with sandy soils typical of sandstone and alluvium were characterized by slow growth rates, shade tolerance, evergreen leaves, and high wood density, traits allowing persistence on resource-poor soils. In contrast, fast-growing pioneer species rarely occurred on sandy soils, except for Lophira alata.Conclusions/significanceThe results indicate strong environmental filtering due to differential soil resource availability across geological substrates. Additionally, long-term human disturbances in resource-rich areas may have accentuated the observed patterns of species and trait distributions. Trait differences across geological substrates imply pronounced differences in population and ecosystem processes, and call for different conservation and management strategies.

Dataset Information

Biotic Interactions Shape the Ecological Distributions of Staphylococcus Species.

Importance

Publications

Biotic Interactions Shape the Ecological Distributions of Staphylococcus Species.

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