Biotic Interactions Shape the Ecological Distributions of <italic toggle="yes">Staphylococcus</italic> 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 cou...

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Autores principales:	Erik K. Kastman, Noelani Kamelamela, Josh W. Norville, Casey M. Cosetta, Rachel J. Dutton, Benjamin E. Wolfe
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/3b293b242c9e4dd583c4f087720f8fe2
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spelling	oai:doaj.org-article:3b293b242c9e4dd583c4f087720f8fe22021-11-15T15:50:16ZBiotic Interactions Shape the Ecological Distributions of <italic toggle="yes">Staphylococcus</italic> Species10.1128/mBio.01157-162150-7511https://doaj.org/article/3b293b242c9e4dd583c4f087720f8fe22016-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01157-16https://doaj.org/toc/2150-7511ABSTRACT 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.Erik K. KastmanNoelani KamelamelaJosh W. NorvilleCasey M. CosettaRachel J. DuttonBenjamin E. WolfeAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 5 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Erik K. Kastman Noelani Kamelamela Josh W. Norville Casey M. Cosetta Rachel J. Dutton Benjamin E. Wolfe Biotic Interactions Shape the Ecological Distributions of <italic toggle="yes">Staphylococcus</italic> Species
description	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.
format	article
author	Erik K. Kastman Noelani Kamelamela Josh W. Norville Casey M. Cosetta Rachel J. Dutton Benjamin E. Wolfe
author_facet	Erik K. Kastman Noelani Kamelamela Josh W. Norville Casey M. Cosetta Rachel J. Dutton Benjamin E. Wolfe
author_sort	Erik K. Kastman
title	Biotic Interactions Shape the Ecological Distributions of <italic toggle="yes">Staphylococcus</italic> Species
title_short	Biotic Interactions Shape the Ecological Distributions of <italic toggle="yes">Staphylococcus</italic> Species
title_full	Biotic Interactions Shape the Ecological Distributions of <italic toggle="yes">Staphylococcus</italic> Species
title_fullStr	Biotic Interactions Shape the Ecological Distributions of <italic toggle="yes">Staphylococcus</italic> Species
title_full_unstemmed	Biotic Interactions Shape the Ecological Distributions of <italic toggle="yes">Staphylococcus</italic> Species
title_sort	biotic interactions shape the ecological distributions of <italic toggle="yes">staphylococcus</italic> species
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/3b293b242c9e4dd583c4f087720f8fe2
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Biotic Interactions Shape the Ecological Distributions of <italic toggle="yes">Staphylococcus</italic> Species

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