Rapid shifts in Atta cephalotes fungus-garden enzyme activity after a change in fungal substrate (Attini, Formicidae)
ABSTRACT Fungus gardens of the basidiomycete Leucocoprinus gongylophorus sustain large colonies of leaf-cutting ants by degrading the plant material collected by the ants. Recent studies have shown that enzyme activity in these gardens is primarily targeted toward starch, proteins and the pectin matrix associated with cell walls, rather than toward structural cell wall components such as cellulose and hemicelluloses. Substrate constituents are also known to be sequentially degraded in different sections of the fungus garden. To test the plasticity in the extracellular expression of fungus-garden enzymes, we measured the changes in enzyme activity after a controlled shift in fungal substrate offered to six laboratory colonies of Atta cephalotes. An ant diet consisting exclusively of grains of parboiled rice rapidly increased the activity of endo-proteinases and some of the pectinases attacking the backbone structure of pectin molecules, relative to a pure diet of bramble leaves, and this happened predominantly in the most recently established top sections of fungus gardens. However, fungus-garden amylase activity did not significantly increase despite the substantial increase in starch availability from the rice diet, relative to the leaf diet controls. Enzyme activity in the older, bottom sections of fungus gardens decreased, indicating a faster processing of the rice substrate compared to the leaf diet. These results suggest that leaf-cutting ant fungus gardens can rapidly adjust enzyme activity to provide a better match with substrate availability and that excess starch that is not protected by cell walls may be digested by the ants rather than by the fungus-garden symbiont.
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Full-textDOI: · Available from: Pepijn Wilhelmus Kooij, May 28, 2015
SourceAvailable from: Jacobus J Boomsma[Show abstract] [Hide abstract]
ABSTRACT: Background Cooperative benefits of mutualistic interactions are affected by genetic variation among the interacting partners, which may have consequences for interaction-specificities across guilds of sympatric species with similar mutualistic life histories. The gardens of fungus-growing (attine) ants produce carbohydrate active enzymes that degrade plant material collected by the ants and offer them food in exchange. The spectrum of these enzyme activities is an important symbiont service to the host but may vary among cultivar genotypes. The sympatric occurrence of several Trachymyrmex and Sericomyrmex higher attine ants in Gamboa, Panama provided the opportunity to do a quantitative study of species-level interaction-specificity.ResultsWe genotyped the ants for Cytochrome Oxidase and their Leucoagaricus fungal cultivars for ITS rDNA. Combined with activity measurements for 12 carbohydrate active enzymes, these data allowed us to test whether garden enzyme activity was affected by fungal strain, farming ants or combinations of the two. We detected two cryptic ant species, raising ant species number from four to six, and we show that the 38 sampled colonies reared a total of seven fungal haplotypes that were different enough to represent separate Leucoagaricus species. The Sericomyrmex species and one of the Trachymyrmex species reared the same fungal cultivar in all sampled colonies, but the remaining four Trachymyrmex species largely shared the other cultivars. Fungal enzyme activity spectra were significantly affected by both cultivar species and farming ant species, and more so for certain ant-cultivar combinations than others. However, relative changes in activity of single enzymes only depended on cultivar genotype and not on the ant species farming a cultivar.Conclusions Ant cultivar symbiont-specificity varied from almost full symbiont sharing to one-to-one specialization, suggesting that trade-offs between enzyme activity spectra and life-history traits such as desiccation tolerance, disease susceptibility and temperature sensitivity may apply in some combinations but not in others. We hypothesize that this may be related to ecological specialization in general, but this awaits further testing. Our finding of both cryptic ant species and extensive cultivar diversity underlines the importance of identifying all species-level variation before embarking on estimates of interaction specificity.BMC Evolutionary Biology 12/2014; 14(1):244. DOI:10.1186/s12862-014-0244-6 · 3.41 Impact Factor
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ABSTRACT: Molecular studies have added significantly to understanding of the role of fungi and fungal enzymes in the efficient biomass conversion, which takes place in the fungus garden of leaf-cutting ants. It is now clear that the fungal symbiont expresses the full spectrum of genes for degrading cellulose and other plant cell wall polysaccharides. Since the start of the genomics era, numerous interesting studies have especially focused on evolutionary, molecular, and organismal aspects of the biological and biochemical functions of the symbiosis between leaf-cutting ants (Atta spp. and Acromyrmex spp.) and their fungal symbiont Leucoagaricus gongylophorus. Macroscopic observations of the fungus-farming ant colony inherently depict the ants as the leading part of the symbiosis (the myrmicocentric approach, overshadowing the mycocentric aspects). However, at the molecular level, it is fungal enzymes that enable the ants to access the nutrition embedded in recalcitrant plant biomass. Our hypothesis is that the evolutionary events that established fungus-farming practice were predisposed by a fascinating fungal evolution toward increasing attractiveness to ants. This resulted in the ants allowing the fungus to grow in the nests and began to supply plant materials for more fungal growth. Molecular studies also confirm that specialized fungal structures, the gongylidia, with high levels of proteins and rich blend of enzymes, are essential for symbiosis. Harvested and used as ant feed, the gongylidia are the key factor for sustaining the highly complex leaf-cutting ant colony. This microbial upgrade of fresh leaves to protein-enriched animal feed can serve as inspiration for modern biorefinery technology.Applied Microbiology and Biotechnology 04/2014; 98(11). DOI:10.1007/s00253-014-5708-5 · 3.81 Impact Factor
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ABSTRACT: Fungus-gardening insects are among the most complex organisms due to their extensive coevolutionary histories with obligate fungal symbionts and other microbes.Some fungus-gardening insect lineages share fungal symbionts with other members of their lineage and thus exhibit diffuse co-evolutionary relationships, while others exhibit little or no symbiont sharing, resulting in host-fungus fidelity. The mechanisms that maintain this symbiont fidelity are currently unknown. Prior work suggested that derived leaf-cutting ants in the genus Atta interact synergistically with leaf-cutter fungi ('Attamyces') by exhibiting higher fungal growth rates and enzymatic activities than when growing a fungus from the sister-clade to Attamyces (so-called 'Trachymyces') grown primarily by the non-leaf cutting Trachymyrmex ants that form, correspondingly, the sister-clade to leafcutting ants. To elucidate the enzymatic bases of host-fungus specialization in leafcutting ants, we conducted a reciprocal fungus-switch experiment between the ant Atta texana and the ant Trachymyrmex arizonensis and report measured enzymatic activities of switched, and sham-switched fungus gardens to digest starch, pectin, xylan, cellulose, and casein. Gardens exhibited higher amylase and pectinase activities when A. texana ants cultivated Attamyces compared to Trachymyces fungi, consistent with enzymatic specialization. In contrast, gardens showed comparable amylase and pectinase activities when T. arizonensis cultivated either fungal species. Although gardens of leaf-cutting ants are not known to be significant metabolizers of cellulose, T. arizonensis were able to maintain gardens with significant cellulase activity when growing either fungal species. In contrast to carbohydrate metabolism, protease activity was significantly higher in Attamyces than in Trachymyces, regardless of the ant host. Activity of some enzymes employed by this symbiosis therefore arises from complex interactions between ant-host and fungal-symbiont.Journal of Experimental Biology 05/2014; 217(14). DOI:10.1242/jeb.098483 · 3.00 Impact Factor