Reconstructing the functions of endosymbiotic Mollicutes in fungus-growing ants.

Panagiotis Sapountzis,Morten Schiott,Mariya Zhukova,Jonathan Z Shik,Jacobus J Boomsma

doi:10.7554/elife.39209

Abstract

Mollicutes, a widespread class of bacteria associated with animals and plants, were recently identified as abundant abdominal endosymbionts in healthy workers of attine fungus-farming leaf-cutting ants. We obtained draft genomes of the two most common strains harbored by Panamanian fungus-growing ants. Reconstructions of their functional significance showed that they are independently acquired symbionts, most likely to decompose excess arginine consistent with the farmed fungal cultivars providing this nitrogen-rich amino-acid in variable quantities. Across the attine lineages, the relative abundances of the two Mollicutes strains are associated with the substrate types that foraging workers offer to fungus gardens. One of the symbionts is specific to the leaf-cutting ants and has special genomic machinery to catabolize citrate/glucose into acetate, which appears to deliver direct metabolic energy to the ant workers. Unlike other Mollicutes associated with insect hosts, both attine ant strains have complete phage-defense systems, underlining that they are actively maintained as mutualistic symbionts.

Highlights

Bacterial endosymbionts, defined here as comprising both intra- and extra-cellular symbionts (Bourtzis and Miller, 2006), occur in all eukaryotic lineages and range from parasites to mutualists (Bourtzis and Miller, 2006; Martin et al, 2017)
At the Panama site where we conducted our study, the EntAcro1 and EntAcro10 symbionts are the most common Entomoplasmatales strains associated with attine ants and they represent the majority of sequence reads (>40% jointly for both EntAcro symbionts that were obtained from these ants in field colonies and >50% in captive colonies fed ad libitum; Sapountzis et al, 2015)
Our study captured much of the qualitative and quantitative biodiversity of abdominal Mollicutes endosymbionts. We show that these two symbionts are phylogenetically distant and evolved independently (Figure 1), but that their gene contents reflect convergent adjustment to life as ant symbionts when compared to related Mesoplasma and Spiroplasma bacteria associated with other arthropods or plants (Figure 1—figure supplement 3)

Summary

Introduction

Bacterial endosymbionts, defined here as comprising both intra- and extra-cellular symbionts (Bourtzis and Miller, 2006), occur in all eukaryotic lineages and range from parasites to mutualists (Bourtzis and Miller, 2006; Martin et al, 2017). Their genomes tend to evolve faster than those of free-living bacteria (Delaney et al, 2012; Moran et al, 1995) and they often rely on recombination and horizontal gene transfer when their tissue localizations allow frequent DNA exchange with other bacteria, which tends to purge deleterious mutations when effective population sizes are small (Naito and Pawlowska, 2016; Takeuchi et al, 2014). In such cases natural selection is expected to have purged any genes that mediated functions that could be provided more productively by the hosts, a process that has been referred to as Black-Queen dynamics (Morris et al, 2012)

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Conclusion