The Hyphosphere of Leaf-Cutting Ant Cultivars Is Enriched with Helper Bacteria

Martiarena, Maria Jesus Sutta; Deveau, Aurélie; Montoya, Quimi Vidaurre; Flórez, Laura; Rodrigues, André

doi:10.1007/s00248-023-02187-w

Cited by 6 publications

(5 citation statements)

References 47 publications

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“…Five OTUs were identified as core members of pellet communities in all four ant species sampled: Moraxella (OTU14), Staphylococcus (OTU15), Lawsonella (OTU20), Pelomonas (OTU21), and Micrococcus (OTU27) (S4 Table). None of these five have been previously identified as fungus-growing ant symbionts, but Staphylococcus has been found in earlier fungal garden studies (22,23,46). We found no significant pairwise differences in garden microbiota between species aside from between M. mikromelanos and Ac.…”

Section: Resultsmentioning

confidence: 92%

“…Pelomonas (OTU 21) is closely related to bacterial OTUs from a variety of sources, but particularly relevant in the context of our study is the association of this bacterial genus with fungal gardens of Mycocepurus goeldii (54) and the males of Trachymyrmex septentrionalis (25). Staphylococcus may function to increase bioavailable iron and promote growth of the fungal cultivar (46). In general, these bacterial genera are closely related to human-associated or environmentally abundant isolates.…”

Section: Discussionmentioning

confidence: 99%

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Vertical transmission of fungus-growing ant microbiota is species-specific and constrained by queens

Sadowski,

Sapountzis,

Kooij

et al. 2024

Preprint

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Multipartite symbioses are inherently complex, involving dynamic ecological interactions between organisms with intertwined yet distinct evolutionary histories. The fungus-growing (attine) ants facilitate maintenance of a symbiotic species network through maternal vertical transmission of an obligate fungal symbiont. While the gut microbiomes of fungus-growing ant species are remarkably simple, their fungal gardens support diverse microbial communities. Here, we focus on an understudied transmission bottleneck: the fungal garden pellet that nest-founding queens transfer to inoculate a new fungal garden. We used 16S rRNA metagenomic sequencing to reconstruct the extent of vertical transmission of bacteria to new gardens via queen pellets in four sympatric fungus-growing ant species (Atta sexdens,Atta cephalotes,Acromyrmex echinatior, andMycetomoellerius mikromelanos) from Central Panama. We also characterized the bacterial communities associated with queen eggs and somatic tissues (mesosomas, guts and ovaries) to assess whether queens are likely to transmit symbiotic bacteria of workers, such as cuticular Actinobacteria and endosymbionts (Wolbachia,Mesoplasma, andSpiroplasma). Our results suggest that garden-associated bacteria are mainly horizontally acquired as the bacterial communities of pellets shared few bacterial taxa with the mature gardens of the four ant species investigated. While the bacterial communities of garden pellets showed some species-specificity, a subset of prevalent bacterial taxa were shared across ant species. Further, our findings provide evidence for vertical transmission of species-specific endosymbiotic bacteria through a transovarial route and/or via fecal droplets. Overall, while we found mixed evidence for vertical transmission of garden bacteria, our results support maternal transmission as a primary route for gut-associated symbionts. While our results suggest that vertical transmission of fungus-growing ant bacterial associates is mediated by the ant hosts, the mechanism behind this host control is not yet understood.

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Section: Resultsmentioning

confidence: 92%

Section: Discussionmentioning

confidence: 99%

Vertical transmission of fungus-growing ant microbiota is species-specific and constrained by queens

Sadowski,

Sapountzis,

Kooij

et al. 2024

Preprint

View full text Add to dashboard Cite

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“…This is analogous to what has previously been observed in plants (Trivedi et al ., 2020), animals (Hildebrand et al ., 2013; Goodrich et al ., 2016) and more recently in fungal fruiting bodies (Gohar et al ., 2022) whereby host genetics are a main driver of microbiome community structure. Given that the study of fungi‐associated bacteria is a growing field of research (Martiarena et al ., 2023; Wang et al ., 2023), this work provides important insights into how fungal microbiomes are assembled. Future research could attempt to quantify the proportion of endobacterial community variation that is explained by the fungal host genotype as compared to the influence of environmental factors, which are themselves known to impact AMF communities.…”

Section: Discussionmentioning

confidence: 99%

Spores of arbuscular mycorrhizal fungi host surprisingly diverse communities of endobacteria

Lastovetsky,

Caruso,

Brennan

et al. 2024

New Phytologist

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Summary Arbuscular mycorrhizal fungi (AMF) are ubiquitous plant root symbionts, which can house two endobacteria: Ca. Moeniiplasma glomeromycotorum (CaMg) and Ca. Glomeribacter gigasporarum (CaGg). However, little is known about their distribution and population structure in natural AMF populations and whether AMF can harbour other endobacteria. We isolated AMF from two environments and conducted detailed analyses of endobacterial communities associated with surface‐sterilised AMF spores. Consistent with the previous reports, we found that CaMg were extremely abundant (80%) and CaGg were extremely rare (2%) in both environments. Unexpectedly, we discovered an additional and previously unknown level of bacterial diversity within AMF spores, which extended beyond the known endosymbionts, with bacteria belonging to 10 other phyla detected across our spore data set. Detailed analysis revealed that: CaGg were not limited in distribution to the Gigasporaceae family of AMF, as previously thought; CaMg population structure was driven by AMF host genotype; and a significant inverse correlation existed between the diversity of CaMg and diversity of all other endobacteria. Based on these data, we generate novel testable hypotheses regarding the function of CaMg in AMF biology by proposing that they might act as conditional mutualists of AMF.

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“…This functional polyploidy combined with limited accuracy of existing genomes have precluded studies of changes in genome synteny as well as structural variation within haplotypes. For instance, the short-read L. gongylophorus genome of Aylward et al (2013) isolated from a Panamanian colony of Atta cephalotes provides the most current and best cited for genome for this fungal species (Floudas et al, 2015; Dentinger et al, 2016; Nygaard et al, 2016; Guo et al, 2023; Martiarena et al, 2023). While the Aylward et al (2013) genome was the state of the art at the time of its publication, it provides an incomplete and fragmented assembly that cannot delimit key features of genomic change.…”

Section: Introductionmentioning

confidence: 99%

Genomic Signatures of Domestication in a Fungus Obligately Farmed by Leafcutter Ants

Leal-Dutra,

Vizueta,

Baril

et al. 2024

Preprint

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The naturally selected fungal crop (Leucoagaricus gongylophorus) farmed by leafcutter ants shows striking parallels with artificially selected plant crops domesticated by humans (e.g., polyploidy, engorged nutritional rewards, dependence on cultivation). To date, poorly resolvedL. gongylophorusgenomes based on short-read sequencing have constrained hypotheses about how millions of years under cultivation by ants shaped the fungal crop genome and potentially drove domestication. We use PacBio HiFi sequencing ofL. gongylophorusfrom the leafcutter antAtta colombicato identify 18 putatively novel biosynthetic gene clusters that likely cemented life as a cultivar (e.g., plant fragment degradation, ant-farmer communication, antimicrobial defense). Comparative analyses with cultivated and free-living fungi showed genomic signatures of stepwise domestication transitions: 1) free-living to ant-cultivated: loss of genes conferring stress response and detoxification, 2) hyphal food to engorged nutritional rewards: expansions of genes governing cellular homeostasis, carbohydrate metabolism, and siderophore biosynthesis, and 3) detrital provisioning to freshly cut plant fragments: gene expansions promoting cell wall biosynthesis, fatty acid metabolism, and DNA repair. Comparisons acrossL. gongylophorusfungi farmed by three leafcutter ant species highlight genomic signatures of exclusively vertical clonal propagation and widespread transposable element activity. These results show how natural selection can shape domesticated cultivar genomes towards long-term ecological resilience of farming systems that have thrived across millennia.

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The Hyphosphere of Leaf-Cutting Ant Cultivars Is Enriched with Helper Bacteria

Cited by 6 publications

References 47 publications

Vertical transmission of fungus-growing ant microbiota is species-specific and constrained by queens

Vertical transmission of fungus-growing ant microbiota is species-specific and constrained by queens

Spores of arbuscular mycorrhizal fungi host surprisingly diverse communities of endobacteria

Genomic Signatures of Domestication in a Fungus Obligately Farmed by Leafcutter Ants

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