The evolution of abdominal microbiomes in fungus-growing ants

The attine ants are a monophyletic lineage that switched to fungus-farming ca. 55-60 MYA. They have become a model for the study of complex symbioses after additional fungal and bacterial symbionts were discovered, but their abdominal endosymbiotic bacteria remain largely unknown. Here we present a comparative microbiome analysis of endosymbiotic bacteria spanning the entire phylogenetic tree. We show that, across 17 representative sympatric species from eight genera sampled in Panama, abdominal microbiomes are dominated by Mollicutes, α- and γ-Proteobacteria, and Actinobacteria. Bacterial abundances increase from basal to crown branches in the phylogeny reflecting a shift towards putative specialized and abundant abdominal microbiota after the ants domesticated gongylidia-bearing cultivars, but before the origin of industrial-scale farming based on leaf-cutting herbivory. This transition coincided with the ancestral single colonization event of Central/North America ca. 20 MYA, documented in a recent phylogenomic study showing that the entire crown-group of the higher attine ants, including the leaf-cutting ants, evolved there and not in South America. Several bacterial species are located in gut tissues or abdominal organs of the evolutionarily derived, but not the basal attine ants. The composition of abdominal microbiomes appears to be affected by the presence/absence of defensive antibiotic-producing actinobacterial biofilms on the worker ants’ cuticle, but the significance of this association remains unclear. The patterns of diversity, abundance, and sensitivity of the abdominal microbiomes that we obtained explore novel territory in the comparative analysis of attine fungus-farming symbioses and raise new questions for further in-depth research.

切叶蚁亚科蚂蚁（Attinae ants）是一个单系类群，其真菌种植行为大约起源于5500万至6000万年前。在发现更多真菌与细菌共生体后，该类群已成为研究复杂共生关系的经典模型，但学界对其腹部内共生细菌的认知仍十分有限。本研究对覆盖整个系统发育树的腹部内共生细菌开展了比较微生物组分析。研究团队对巴拿马地区8个属的17个代表性同域物种进行采样分析后发现，其腹部微生物组主要由柔膜菌纲（Mollicutes）、α-变形菌纲（α-Proteobacteria）、γ-变形菌纲（γ-Proteobacteria）以及放线菌门（Actinobacteria）构成。系统发育树中，细菌丰度从基部分支向冠群分支逐渐升高，这一变化反映出：在蚂蚁驯化携带有真菌膨大体（gongylidia）的栽培真菌菌株之后、基于切叶植食的工业化真菌种植起源之前，蚂蚁腹部微生物组逐渐向推测的特化且高丰度的状态转变。这一演化转变与约2000万年前蚂蚁祖先单次殖民中美洲/北美洲的事件相吻合，近期一项系统基因组学研究证实，包括切叶蚁在内的所有高等切叶蚁冠群均演化自该区域，而非南美洲。部分细菌物种仅存在于演化衍生类群（而非基部类群）切叶蚁的肠道组织或腹部器官中。腹部微生物组的组成似乎受工蚁体表是否存在产抗生素放线菌生物膜的影响，但二者关联的生物学意义仍有待阐明。本研究揭示的腹部微生物组多样性、丰度与敏感性模式，为切叶蚁真菌种植共生关系的比较分析开辟了全新研究领域，并为后续深入研究提出了新的科学问题。