Metagenomics Reveals Diet-Specific Specialization of Bacterial Communities in Fungus Gardens of Grass- and Dicot-Cutter Ants

Abstract

Leaf-cutter ants in the genus Atta are dominant herbivores in the Neotropics. While most species of Atta cut dicots to incorporate into their fungus gardens, some species specialize on grasses. Here we examine the bacterial community associated with the fungus gardens of grass-and dicot-cutter ants to examine how changes in substrate input affect the bacterial community. We sequenced the metagenomes of 12 Atta fungus gardens, across four species of ants, with a total of 5.316 Gbp of sequence data. We show significant differences in the fungus garden bacterial community composition between dicot-and grass-cutter ants, with grass-cutter ants having lower diversity. Reflecting this difference in community composition, the bacterial functional profiles between the fungus gardens are significantly different. Specifically, grass-cutter ant fungus garden metagenomes are particularly enriched for genes responsible for amino acid, siderophore, and terpenoid biosynthesis while dicot-cutter ant fungus gardens metagenomes are enriched in genes involved in membrane transport. Differences between community composition and functional capacity of the bacteria in the two types of fungus gardens reflect differences in the substrates that the ants incorporated. These results show that different substrate inputs matter for fungus garden bacteria and shed light on the potential role of bacteria in mediating the ants' transition to the use of a novel substrate.

A domesticated fungal cultivar recycles its cytoplasmic contents as nutritional rewards for its leafcutter ant farmers

“…Second, nutrients also appear to derive from bacterial symbionts (rather than plant fragments or autophagic recycling) (68)(69)(70). For instance, attine ants have lost the ability to synthesize arginine (71)-and depend on the cultivar's metabolism to produce this nitrogen-rich amino acid (26).…”

Lessons From Insect Fungiculture: From Microbial Ecology to Plastics Degradation

“…By cultivating lignocellulolytic fungal crops, these insect-fungus symbioses are notorious organic matter decomposers, influencing energy and nutrient dynamics over spatial and temporal scales ( Abbadie and Lepage, 1989 ; Jones, 1990 ; Verchot et al, 2003 ; Jouquet et al, 2011 ; Crowther et al, 2012 ; Siegert et al, 2018 ; Šamonil et al, 2020 ). Insects agricultural systems are also inhabited by characteristic, convergent, and adapted microbiota, that appear to integrate pathways for the detoxification of plant defensive metabolites and lignocellulose degradation ( Suen et al, 2010 ; Aylward et al, 2014 ; Poulsen et al, 2014 ; Barcoto et al, 2020 ; Francoeur et al, 2020 ; Khadempour et al, 2020 ). The microbiota abundantly encodes genes for xenobiotics modification, such as pathways for polycyclic aromatic carbon and alkane degradation, though the role of these routes are not clear ( Barcoto et al, 2020 ).…”

“…Despite having lost an ancestral ligninase domain, L. gongylophorus encodes for laccases, glyoxal oxidases, cellulases (GH6, GH7, GH9), hemicellulases and pectinases (CE5, CE8, GH15, GH28, and PL1; Aylward et al, 2013 ; Nygaard et al, 2016 ). The garden microbiota, dominated by Enterobacter , Klebsiella, Pantoea, Pseudomonas , and Serratia , encode for metabolic pathways that could compliment the fungal metabolism ( Scott et al, 2010 ; Suen et al, 2010 ; Aylward et al, 2012 ; Barcoto et al, 2020 ; Francoeur et al, 2020 ; Khadempour et al, 2020 ).…”

Burkholderiafrom fungus gardens of fungus-growing ants produce antifungals that inhibit the specialized parasiteEscovopsis

“…principally degrades the substrate and produces usable energy for the ants (12,13). In addition, a consistent bacterial community composed primarily of Proteobacteria exists within fungus gardens (14)(15)(16)(17)(18). In leaf-cutter ants, the bacterial community has been shown to help degrade plant secondary compounds and aid in nitrogen acquisition for the ant .…”