title: Microbes are trophic analogs of animals.
abstract: In most ecosystems, microbes are the dominant consumers, commandeering much of the heterotrophic biomass circulating through food webs. Characterizing functional diversity within the microbiome, therefore, is critical to understanding ecosystem functioning, particularly in an era of global biodiversity loss. Using isotopic fingerprinting, we investigated the trophic positions of a broad diversity of heterotrophic organisms. Specifically, we examined the naturally occurring stable isotopes of nitrogen ((15)N:(14)N) within amino acids extracted from proteobacteria, actinomycetes, ascomycetes, and basidiomycetes, as well as from vertebrate and invertebrate macrofauna (crustaceans, fish, insects, and mammals). Here, we report that patterns of intertrophic (15)N-discrimination were remarkably similar among bacteria, fungi, and animals, which permitted unambiguous measurement of consumer trophic position, independent of phylogeny or ecosystem type. The observed similarities among bacterial, fungal, and animal consumers suggest that within a trophic hierarchy, microbiota are equivalent to, and can be interdigitated with, macrobiota. To further test the universality of this finding, we examined Neotropical fungus gardens, communities in which bacteria, fungi, and animals are entwined in an ancient, quadripartite symbiosis. We reveal that this symbiosis is a discrete four-level food chain, wherein bacteria function as the apex carnivores, animals and fungi are meso-consumers, and the sole herbivores are fungi. Together, our findings demonstrate that bacteria, fungi, and animals can be integrated within a food chain, effectively uniting the macro- and microbiome in food web ecology and facilitating greater inclusion of the microbiome in studies of functional diversity.
authors.affiliation: Department of Entomology, University of Wisconsin, Madison, WI 53706; US Department of Agriculture-Agricultural Research Service, University of Wisconsin, Madison, WI 53706; steffan@entomology.wisc.edu.
authors.forename: Shawn A
authors.initials: SA
authors.lastname: Steffan
authors.affiliation: Department of Biogeochemistry, Japan Agency for Marine-Earth Science and Technology, Yokosuka 237-0061, Japan;
authors.forename: Yoshito
authors.initials: Y
authors.lastname: Chikaraishi
authors.affiliation: Department of Bacteriology, University of Wisconsin, Madison, WI 53706;
authors.forename: Cameron R
authors.initials: CR
authors.lastname: Currie
authors.affiliation: Department of Bacteriology, University of Wisconsin, Madison, WI 53706;
authors.forename: Heidi
authors.initials: H
authors.lastname: Horn
authors.affiliation: Department of Entomology, University of Wisconsin, Madison, WI 53706;
authors.forename: Hannah R
authors.initials: HR
authors.lastname: Gaines-Day
authors.affiliation: Department of Forest & Wildlife Ecology, University of Wisconsin, Madison, WI 53706.
authors.forename: Jonathan N
authors.initials: JN
authors.lastname: Pauli
authors.affiliation: US Department of Agriculture-Agricultural Research Service, University of Wisconsin, Madison, WI 53706;
authors.forename: Juan E
authors.initials: JE
authors.lastname: Zalapa
authors.affiliation: Department of Biogeochemistry, Japan Agency for Marine-Earth Science and Technology, Yokosuka 237-0061, Japan;
authors.forename: Naohiko
authors.initials: N
authors.lastname: Ohkouchi
mesh_terms: D000818:Animals; D017753:Ecosystem; D064307:Microbiota
keywords: compound specific; food chain; leaf-cutter ant; microbe; stable isotope