Various insects engage in microbial mutualisms in which the reciprocal benefits exceed the costs. Ants of the genus Camponotus benefit from nutrient supplementation by their mutualistic endosymbiotic bacteria, Blochmannia, but suffer a cost in tolerating and regulating the symbiont. This cost suggests that the ants face secondary consequences such as susceptibility to pathogenic infection and transmission. In order to elucidate the symbiont’s effects on development and disease defence, Blochmannia floridanus was reduced in colonies of Camponotus floridanus using antibiotics. Colonies with reduced symbiont levels exhibited workers of smaller body size, smaller colony size, and a lower major-to-minor worker caste ratio, indicating the symbiont’s crucial role in development. Moreover, these ants had decreased cuticular melanisation, yet higher resistance to the entomopathogen Metarhizium brunneum, suggesting that the symbiont reduces the ants’ ability to fight infection, despite the availability of melanin to aid in mounting an immune response. While the benefits of improved growth and development likely drive the mutualism, the symbiont imposes a critical trade-off. The ants’ increased susceptibility to infection exacerbates the danger of pathogen transmission, a significant risk given ants’ social lifestyle. Thus, the results warrant research into potential adaptations of the ants and pathogens that remedy and exploit the described disease vulnerability.

Milk fermentation has a rich history in which food culture, the environment, and microbes intersect. However, traditional practices and their associated microbes have largely been replaced by industrial processes. We investigate a historical fermentation originating from Turkey and Bulgaria – ant yogurt. By examining the traditional practice, gastronomic applications, and experimentally derived yogurts, we uncover that the red wood ant holobiont facilitates fermentation. Bacteria hosted by the ants can proliferate in the milk. Specifically, live ants contribute lactic and acetic acid bacteria, including Frutilactobacillus sanfranciscensis, normally related to sourdough. Consequently, the bacterial community introduces lactic and acetic acid, while the ants provide formic acid, collectively advantageous for yogurt acidification and coagulation. Last, the ants and bacteria produce potential casein-active proteases that may further alter the yogurt texture. Our findings highlight the value of integrating traditional and biological frameworks to uncover the origins and applications of fermented food microbes.

Mutualistic coevolution can be mediated by vertical transmission of symbionts between host generations. Termites host complex gut bacterial communities with evolutionary histories indicative of mixed-mode transmission. Here, we document that vertical transmission of gut bacterial strains is congruent across parent to offspring colonies in four pedigrees of the fungus-farming termite Macrotermes natalensis . We show that 44% of the offspring colony microbiome, including more than 80 bacterial genera and pedigree-specific strains, are consistently inherited. We go on to demonstrate that this is achieved because colony-founding reproductives are selectively enriched with a set of non-random, environmentally sensitive and termite-specific gut microbes from their colonies of origin. These symbionts transfer to offspring colony workers with high fidelity, after which priority effects appear to influence the composition of the establishing microbiome. Termite reproductives thus secure transmission of complex communities of specific, co-evolved microbes that are critical to their offspring colonies. Extensive yet imperfect inheritance implies that the maturing colony benefits from acquiring environmental microbes to complement combinations of termite, fungus and vertically transmitted microbes; a mode of transmission that is emerging as a prevailing strategy for hosts to assemble complex adaptive microbiomes.

Summary: Milk fermentation has a rich history in which food culture, the environment, and microbes intersect. However, the biocultural origins of fermentation practices and microbes have largely been replaced by industrial processes. Here, we consider a historical fermentation originating from Turkey and Bulgaria – ant yogurt. We revisit the traditional practices and modern gastronomic applications that use red wood ants ( Formica rufa group) to initiate milk fermentation. Subsequently, we characterize the ants and experimental ant-derived yogurts. We uncover that the ant holobiont, which consists of the ants and their microbes, contributes key acids and enzymes to fermentation. Metabarcoding and culturing revealed that lactic and acetic acid bacteria, including species related to conventional sourdough, originate from the live ants and proliferate in the milk. The ants and bacteria consequently introduce formic, lactic, and acetic acid, advantageous for yogurt acidification and coagulation. Last, proteases with the potential to act on casein may alter yogurt texture and are produced by the ants and bacteria. The ant holobiont thus catalyses fermentation akin to the microbial consortia in other ferments. Our findings highlight the value of integrating traditional, gastronomic, and biological frameworks to uncover the origins and applications of microbes for fermented foods.

Humans have historically relied on acetic acid bacteria (AAB) for food fermentation, yet their origins must trace back to free-living species outside of human environments. In nature, plants, fruit flies, and social insects host AAB. However, the evolutionary transitions of AAB from symbiotic hosts to fermented foods remain ambiguous. Here, we conduct a comprehensive phylogenomic analysis of 570 publicly available AAB genomes. We find that the ∼170My evolutionary history of this group is concordant with the rise of angiosperms, corbiculate bees, and the consequential accelerated availability of environmental carbohydrates. Unlike other ferment-associated microbes, ferment-associated AAB have exclusively evolved from clades inhabiting flowers and fruits, but not insect hosts. Genomic features are similar in plant- and ferment-associated AAB, yet markers of early adaptation to ferments are also present. Conversely, social insect-associated AAB have reduced genome sizes, which may have limited their functional capability to disperse into ferments. Plant- and ferment-associated AAB coincide in the ability to metabolise diverse plant carbohydrates, though both have adapted to produce habitat-specific carbohydrate-active enzymes. In contrast, metabolic capacity is reduced in social insect-associated AAB. By tracing the phylogenomics of this clade, we understand how evolution forged AAB capable of performing metabolic work for humans, shaping the history and potential futures of fermentation.

Mutualistic co-evolution can be mediated by vertical transmission of symbionts between host generations. Organisms exhibit adaptations that ensure optimal microbial inheritance, yet the extent to which this applies to social insects, such as termites that have co-evolved with gut microbes, is poorly resolved. Here, we document consistent vertical transmission across colony generations of fungus-farming termites. Inherited bacteria comprise 44% of the microbiome, over 80 genera, and strains that are specific to termite pedigrees. We show that the superorganism, consisting of reproductives and workers, analogous to gametes and soma of an organism, is adapted to vertically transmit a distinct microbial community with high fidelity. Microbial inheritance is achieved because colony-founding reproductives are endowed with a set of non-random, environmentally-sensitive, and termite-specific gut microbes derived from their colonies of origin. Reproductives biparentally transmit these symbionts to offspring colony workers, where priority effects dictate the composition of the forming colony microbiome. Superorganismal gametes, the reproductives, are thus adapted to secure transmission of entire communities of specific, co-evolved microbes that are critical to the colony microbiome later retained by workers. Extensive vertical transmission aligns with evolutionary patterns of termite-bacterial co-diversification. This colony-level inheritance extends models of transmission from individual organisms to superorganisms, both of which demonstrate adaptations to retain symbiotic fidelity and mixed-mode transmission conducive to mutualism.