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Proc Natl Acad Sci U S A. 2015 Dec 8;112(49):15119-24. doi: 10.1073/pnas.1508782112. Epub 2015 Nov 23.

Microbes are trophic analogs of animals.

Author information

1
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.
2
Department of Biogeochemistry, Japan Agency for Marine-Earth Science and Technology, Yokosuka 237-0061, Japan;
3
Department of Bacteriology, University of Wisconsin, Madison, WI 53706;
4
Department of Entomology, University of Wisconsin, Madison, WI 53706;
5
Department of Forest & Wildlife Ecology, University of Wisconsin, Madison, WI 53706.
6
US Department of Agriculture-Agricultural Research Service, University of Wisconsin, Madison, WI 53706;

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.

KEYWORDS:

compound specific; food chain; leaf-cutter ant; microbe; stable isotope

PMID:
26598691
PMCID:
PMC4679051
DOI:
10.1073/pnas.1508782112
[Indexed for MEDLINE]
Free PMC Article

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