Microbes are trophic analogs of animals

Authors: Steffan, Shawn; CHIKARAISHI, YOSHITO - Japan Agency For Marine-Earth Science And Technology (JAMSTEC); CURRIS, CAMERON - University Of Wisconsin; HORN, HEIDI - University Of Wisconsin; GAINES DAY, HANNAH - University Of Wisconsin; PAULI, JONATHON - University Of Wisconsin; Zalapa, Juan; OHKOUCHI, NAOHIKO - Japan Agency For Marine-Earth Science And Technology (JAMSTEC)

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/15/2015
Publication Date: 12/8/2015
Publication URL: https://handle.nal.usda.gov/10113/61927
Citation: Steffan, S.A., Chikaraishi, Y., Currie, C.R., Horn, H., Gaines Day, H.R., Pauli, J.N., Zalapa, J.E., Ohkouchi, N. 2015. Microbes are trophic analogs of animals. Proceedings of the National Academy of Sciences. 112(49):15119-15124. doi: 10.1073/pnas.1508782112.

Interpretive Summary: Our overarching goal in this work was to provide a basis to accurately interpret the trophic positions of free-roaming heterotrophic organisms, regardless of their phylogenetic or biogeographic origin. We provide empirical evidence that isotopically-derived trophic metrics are equally applicable to animal and microbial consumer groups. Further, we show that fungi are the trophic equivalents of animals, whether they are feeding on plant- or animal-based diets. In a food-web, therefore, mold is meat. Preliminary evidence suggest that the same is true for bacteria. Impact: For food web ecology, this re-frames how microbes, particularly fungi, can be viewed and resolves long-standing questions within the microbiome as to who eats what. This will help to integrate above- and below-ground food webs, and effectively unite macro- and microbiomes under the heterotrophic empire.

Technical Abstract: Plant-based food-webs (‘green food-webs’) have historically been articulated as distinct from detritus-based food-webs (‘brown food-webs’). It has proven difficult to integrate these two spheres using a shared metric because of the difficulties in identifying and quantifying biodiversity within the microbiome. As a result, the trophic ecology of brown food-webs is much less well-understood than that of their green counterparts. Here we characterise the trophic niches of microorganisms by testing how animals and microbes assimilate stable isotopes within specific amino acids. Amino acid isotopic ‘fingerprinting’ provides unprecedented accuracy in the estimation of animal trophic tendency. Using this approach, we measured the isotopic signatures of amino acids extracted from a diversity of fungal species, as well as from crustaceans, fish, insects, and mammals (taxa representing the vast majority of global fauna). Fungal and animal taxa were trophically indistinguishable from one another when fed the same diet. Thus, despite profound phylogenetic disparities, these consumers exhibited similar patterns of isotopic fractionation and were trophically interchangeable, allowing fungi and animals to be interdigitated within food-webs. We brought this approach to bear upon the fungus-gardens of tropical leaf-cutter ants (Acromyrmex), revealing four discrete trophic levels within the fungus-gardens. Our data suggest that leaf-cutter ants are not the dominant herbivores of the Neotropics; rather, it is the fungi they cultivate. Further, the bacteria used by the ants as anti-fungal agents were shown to feed exclusively on the ants, indicating a tightly linked ant-bacterial mutualism. Because amino acid isotopic analysis quantifies trophic position independent of phylogeny, it facilitates unambiguous measurement of trophic function across biological kingdoms, effectively uniting ‘green’ and ‘brown’ food-webs.