Journal Article

Microbes are trophic analogs of animals

Chikaraishi, Yoshito, Steffan, Shawn A, Gaines-Day, Hannah R, Pauli, Jonathan N, Horn, Heidi, Currie, Cameron R, Zalapa, Juan E, Ohkouchi, Naohiko

2015

Overview

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.

• Publisher: National Academy of Sciences,National Acad Sciences
• Subject: Acromyrmex / Actinomycetes / amino acid metabolism / Amino acids / Animals / antifungal agents / Ascomycetes / Bacteria / Basidiomycetes / biodiversity / Biodiversity loss / Biological Sciences / Biomass / Carnivores / Crustacea / Crustaceans / diet / Ecological function / Ecosystem / Ecosystems / fauna / fish / Food webs / fungi / fungus gardens / Herbivores / isotope fractionation / Isotopes / leaf-cutting ants / Macrofauna / mammals / microbiome / Microbiota / Microorganisms / mutualism / niches / Phylogeny / Proteobacteria / Stable isotopes / Symbiosis / tropics