Erratum for Kastman et al., “Biotic Interactions Shape the Ecological Distributions of Staphylococcus Species”

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 coagulasenegative 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. Received 24 June 2016 Accepted 16 September 2016 Published 18 October 2016 Citation Kastman EK, Kamelamela N, Norville JW, Cosetta CM, Dutton RJ, Wolfe BE. 2016. Biotic interactions shape the ecological distributions of Staphylococcus species. mBio 7(5):e01157-16. doi:10.1128/mBio.01157-16. Editor John W. Taylor, University of California Copyright © 2016 Kastman et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. Address correspondence to Benjamin E. Wolfe, benjamin.wolfe@tufts.edu. 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 (1–3). These phylogenetic clusters have been observed in a wide range of environments, from marine microbiomes (4, 5) to our own human microbial landscapes (6). Many widespread bacterial species, including Vibrio, Staphylococcus, and Streptococcus species, commonly co-occur with closely related species or strains (6–8). Explaining these phylogenetic clusters has remained an important puzzle in microbial ecology because theory predicts that competitive exclusion should lead to dominance of only one major lineage when multiple phylogenetically similar lineages co-occur (9, 10). Identifying the ecological processes and molecular mechanisms that shape the distributions of closely related bacterial species can provide important tools to better manage and manipulate microbiomes in agriculture, medicine, and natural ecosystems. Most previous attempts to explain the ecological distributions of bacterial species have focused on the role of abiotic niche partitioning and intraspecific or intrageneric biotic interactions (8, 11, 12), with much of our understanding coming from marine Vibrio species (5, 13–15) and oral biofilms (16, 17). For example, in coastal waters of the Atlantic Ocean, the coexistence of numerous genotypes of several species of Vibrio can be explained by temporal niche partitioning across seasons, preferences for particular microhabitats within seawater, and antagonistic interactions between ecologically defined populations (5, 18). While niche specialization and intraspecific or intrageneric interactions may play important roles in driving coexistence in some microbiomes, biotic interactions between distantly related neighbors that span domains of life could also drive the composition within phylogenetic clusters. For example, in many microbiomes, bacteria coexist with diverse eukaryotic microbes, including fungi (19). Just as different plant species can mediate interactions between closely related insect herbivores that specialize on different RESEARCH ARTICLE