Three phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf‐cutting ants

Zani, Renata de Oliveira Aquino; Ferro, Milene; Bacci, Maurício

doi:10.1002/ece3.8213

Cited by 6 publications

(4 citation statements)

References 70 publications

(94 reference statements)

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“…Our results corroborate previous work suggesting complete transovarial transmission of Wolbachia but not of Entomoplasmatales (e.g, Mesoplasma and Spiroplasma ) in the phylogenetic attine crown group of the leafcutter ants (10). However, contrary to a recent study, which suggested that Atta sexdens from Brazil do not consistently associate with Mesoplasma , we found these bacteria to be a core taxon in the guts of A. sexdens and A. cephalotes queens and/or gynes (50). While Entomoplasmatales symbionts may not be transmitted consistently via eggs, their abundance and prevalence in gardens, worker guts, and queen and gyne guts remains highly relevant.…”

Section: Discussioncontrasting

confidence: 99%

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: Discussioncontrasting

confidence: 99%

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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“…exhibited pronounced antifungal properties; however, the possible symbiotic relationship between harvester ants and actinomycetes remains unclear. The genera Microbacterium isolated from gardens and starter cultures of Atta could play disease-suppressing or other unknown roles [ 8 ], while no specific function was shown for Brachybacterium isolated from the abdomen of Leucocoprinus gongylophorus [ 40 ]. To better understand the ecological role of microorganisms associated with Messor orientalis , it is crucial to analyze the chemical composition and evaluate the biological activity of their metabolites.…”

Section: Discussionmentioning

confidence: 99%

Observation of the Antimicrobial Activities of Two Actinomycetes in the Harvester Ant Messor orientalis

Liu

et al. 2022

Insects

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Observations have shown that seeds collected by harvester ants are less likely to mold. Based on evolutionary analysis and other research, it was hypothesized that harvester ants could apply actinomycetes to protect seeds, similar to the protection of mutualistic fungi by leafcutter ants. Two actinomycetes were successfully isolated from the harvester ant Messor orientalis. The taxonomic status of the actinomycetes was determined by 16S rRNA sequence analysis and biochemical experimental observations. Their inhibitory effects on plant pathogens were measured. One of the bacteria was identified as Brachybacterium phenoliresistens and denoted as B. phenoliresistens MO. The other belonged to the genus Microbacterium. It was named Microbacterium sp. Growth rate determination and coculture experiments were performed to explore the inhibitory effect of actinomycetes on indicator plant pathogens. The inhibition rates of the actinomycetes toward Peronophythora litchii and Rhizoctonia solani were 100% in media containing 30% or more fermentation broth, and they also showed an inhibitory effect on Colletotrichum siamense. The coculture experiment supported this result by showing that the growth of P. litchii and R. solani was inhibited in the presence of actinomycetes. Therefore, the results of this study show the agricultural application potential of these bacteria and may provide a reference for research on the symbiosis of harvester ants with actinomycetes.

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“…Several studies have preliminarily investigated the fungus-growing ant microbiome, primarily focusing on leaf-cutting ants ( 25 – 30 ). These studies show that Acromyrmex and Atta leaf-cutting ants host low-diversity microbiomes that include Wolbachia , Solirubrobacter , Enterobacter , Pseudomonas , and members of the orders Entomoplasmatales and Rhizobiales .…”

Section: Introductionmentioning

confidence: 99%

“…These studies show that Acromyrmex and Atta leaf-cutting ants host low-diversity microbiomes that include Wolbachia , Solirubrobacter , Enterobacter , Pseudomonas , and members of the orders Entomoplasmatales and Rhizobiales . Rhizobiales bacteria contain nif genes that were hypothesized to cycle nitrogen for the ants and their cultivar fungus ( 29 ), as do Methylobacterium , Ralstonia , and Pseudomonas strains ( 30 ). Wolbachia is maternally transmitted in Acromyrmex and Atta ants but lacks a known function.…”

Section: Introductionmentioning

confidence: 99%

Trachymyrmex septentrionalis Ant Microbiome Assembly Is Unique to Individual Colonies and Castes

Green

Klassen

2022

mSphere

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Three phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf‐cutting ants

Abstract: This is an open access article under the terms of the Creat ive Commo ns Attri bution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 6 publications

References 70 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

Observation of the Antimicrobial Activities of Two Actinomycetes in the Harvester Ant Messor orientalis

Trachymyrmex septentrionalis Ant Microbiome Assembly Is Unique to Individual Colonies and Castes

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