Abstract
ABSTRACTMany 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.
Highlights
Many metagenomic sequencing studies have observed the presence of closely related bacterial species or genotypes in the same microbiome
By combining metagenomic data from in situ communities, in vitro reconstructions of experimental communities, and comparative genomics and transcriptomics, we address the following questions. (i) What are the ecological distributions of Staphylococcus species across cheese rind communities and during the development of cheese microbiomes? (ii) What ecological processes, including abiotic and biotic selection, determine the distributions of Staphylococcus species? (iii) Which potential molecular mechanisms underlie these ecological processes? The integrated ecological framework that we develop for dissecting the ecological distributions of these nonpathogenic Staphylococcus species could be applied to pathogenic Staphylococcus species in less-tractable microbiomes
To measure the relative abundances of the four coagulasenegative Staphylococcus (CNS) species previously isolated from cheeses (S. equorum, S. xylosus, S. saprophyticus, and S. succinus), we used whole-genome shotgun metagenomic sequencing of rind microbiomes from 25 cheeses
Summary
Many metagenomic sequencing studies have observed the presence of closely related bacterial species or genotypes in the same microbiome. From the early days of 16S rRNA clone libraries to the current groundswell of high-throughput metagenomics, one common pattern to emerge in studies of microbial community structure is the presence of numerous closely related species or strains of prokaryotes in the same habitat [1,2,3]. These phylogenetic clusters have been observed in a wide range of environments, from marine microbiomes [4, 5] to our own human microbial landscapes [6]. It is unclear if these pairwise interactions dissected in the laboratory can help explain patterns of microbial diversity in multispecies microbial communities found in nature
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