Rediscovering a Forgotten System of Symbiosis: Historical Perspective and Future Potential

Abstract

While the majority of symbiosis research is focused on bacteria, microbial eukaryotes play important roles in the microbiota and as pathogens, especially the incredibly diverse Fungi kingdom. The recent emergence of widespread pathogens in wildlife (bats, amphibians, snakes) and multidrug-resistant opportunists in human populations (Candida auris) has highlighted the importance of better understanding animal–fungus interactions. Regardless of their prominence there are few animal–fungus symbiosis models, but modern technological advances are allowing researchers to utilize novel organisms and systems. Here, I review a forgotten system of animal–fungus interactions: the beetle–fungus symbioses of Drugstore and Cigarette beetles with their symbiont Symbiotaphrina. As pioneering systems for the study of mutualistic symbioses, they were heavily researched between 1920 and 1970, but have received only sporadic attention in the past 40 years. Several features make them unique research organisms, including (1) the symbiont is both extracellular and intracellular during the life cycle of the host, and (2) both beetle and fungus can be cultured in isolation. Specifically, fungal symbionts intracellularly infect cells in the larval and adult beetle gut, while accessory glands in adult females harbor extracellular fungi. In this way, research on the microbiota, pathogenesis/infection, and mutualism can be performed. Furthermore, these beetles are economically important stored-product pests found worldwide. In addition to providing a historical perspective of the research undertaken and an overview of beetle biology and their symbiosis with Symbiotaphrina, I performed two analyses on publicly available genomic data. First, in a preliminary comparative genomic analysis of the fungal symbionts, I found striking differences in the pathways for the biosynthesis of two B vitamins important for the host beetle, thiamine and biotin. Second, I estimated the most recent common ancestor for Drugstore and Cigarette beetles at 8.8–13.5 Mya using sequence divergence (CO1 gene). Together, these analyses demonstrate that modern methods and data (genomics, transcriptomes, etc.) have great potential to transform these beetle–fungus systems into model systems again.

Genome-Wide Analyses of Repeat-Induced Point Mutations in the Ascomycota

“…Class 2 fungi that are apparently asexual included the insect symbiont Sy. buchneri ( Martinson, 2020 ), F. venenatum used in the production of mycoprotein ( Leslie and Summerell, 2006 ), and the plant pathogen F. oxysporum ( Braumann et al, 2008 ).…”

Origin and evolution of fungus farming in wood‐boring Coleoptera – a palaeontological perspective

“…Adult females may, in some cases, cause the death of the trees due to mechanical injury before colonization by the larvae (Wolcott, 1950). The Ptinidae, phylogenetically close relatives of Bostrichidae, have recently been rediscovered in a "forgotten system of symbiosis" with Symbiotaphrina (Ascomycota) (Martinson, 2020). However, this facultative relationship between the symbionts has extracellular and intracellular stages during the life cycle of their beetle hosts and the beetles do not truly farm these fungi.…”

Deciphering the interdependent labyrinth between gut microbiota and the immune system

“…The defined development of the immune system, especially its adaptive nature has concurred with the emergence of a complex microbiome, reflecting an evolving mechanism to maintain a symbiotic relationship with these micro-organisms. Thus, microbes stimulate and calibrate the immune system in all aspects (Martinson 2020).…”