Affiliation:
1. Department of Biology, Tufts University, Medford, Massachusetts, USA
2. Division of Biological Sciences, University of California, San Diego, La Jolla, California, USA
Abstract
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.
Funder
HHS | National Institutes of Health
Tufts University
UC | University of California, San Diego
Publisher
American Society for Microbiology