Lessons From Insect Fungiculture: From Microbial Ecology to Plastics Degradation

Abstract

Anthropogenic activities have extensively transformed the biosphere by extracting and disposing of resources, crossing boundaries of planetary threat while causing a global crisis of waste overload. Despite fundamental differences regarding structure and recalcitrance, lignocellulose and plastic polymers share physical-chemical properties to some extent, that include carbon skeletons with similar chemical bonds, hydrophobic properties, amorphous and crystalline regions. Microbial strategies for metabolizing recalcitrant polymers have been selected and optimized through evolution, thus understanding natural processes for lignocellulose modification could aid the challenge of dealing with the recalcitrant human-made polymers spread worldwide. We propose to look for inspiration in the charismatic fungal-growing insects to understand multipartite degradation of plant polymers. Independently evolved in diverse insect lineages, fungiculture embraces passive or active fungal cultivation for food, protection, and structural purposes. We consider there is much to learn from these symbioses, in special from the community-level degradation of recalcitrant biomass and defensive metabolites. Microbial plant-degrading systems at the core of insect fungicultures could be promising candidates for degrading synthetic plastics. Here, we first compare the degradation of lignocellulose and plastic polymers, with emphasis in the overlapping microbial players and enzymatic activities between these processes. Second, we review the literature on diverse insect fungiculture systems, focusing on features that, while supporting insects' ecology and evolution, could also be applied in biotechnological processes. Third, taking lessons from these microbial communities, we suggest multidisciplinary strategies to identify microbial degraders, degrading enzymes and pathways, as well as microbial interactions and interdependencies. Spanning from multiomics to spectroscopy, microscopy, stable isotopes probing, enrichment microcosmos, and synthetic communities, these strategies would allow for a systemic understanding of the fungiculture ecology, driving to application possibilities. Detailing how the metabolic landscape is entangled to achieve ecological success could inspire sustainable efforts for mitigating the current environmental crisis.

Keywords: bioremediation; lignocellulose; microbiota; plant; pollutants; polymers; symbiosis; xenobiotics.

FIGURE 1

Plant and synthetic polymers degradation (A). Petroleum-derived polyethylene (PE), polypropylene (PP), polystyrene (PS), polyvinylchloride (PVC), polyurethanes (PUR), and polyethylene terephthalate (PET) comprise the majority of plastic polymers currently produced. (B) Despite fundamental differences regarding structure and recalcitrance, lignocellulose and plastic polymers share physical-chemical properties to some extent, that include carbon skeletons with similar chemical bonds, hydrophobic properties, amorphous and crystalline regions. Thus, microbial strategies to deal with such properties would allow enzymes with lignocellulolytic activity to depolymerize plastics. (C) Plastic biodegradation encompasses processes of bio-deterioration and bio-fragmentation. Enzymes active during the biodegradation of synthetic plastic polymers include hydrolases and oxidoreductases. Pencil drawing illustrations by Mariana Barcoto.

FIGURE 2

Insect-fungus mutualism evolved in diverse insect orders. Fungal cultivation by insects may occur in two main configurations: (i) Proto-fungiculture, where insects passively propagate fungi that provide either dietary enrichment, protection against pathogens, or structural reinforcement to the colony/nest, presenting few adaptations to maintain the fungal symbiont. Proto-fungiculture have been observed in the lizard beetle Doubledaya bucculenta and Sirex wood wasps. (ii) Advanced fungiculture, that involve active maintenance of fungal crops by fungus-growing insects, evolving independently in macrotermitine termites, attine ants, platypodinae, and scolytinae beetles. Advanced fungiculture is characterized by high levels of nutritional dependency between fungi and insects fungal crop. Simplified insects phylogeny based on Misof et al. (2014). Pencil drawing illustrations by Mariana Barcoto.

FIGURE 3

Learning from symbioses. To take advantage of microbial flexible and adaptable metabolism, the characterization of both the taxa and the functional profile of the microbiota is required. Designing strategies for biotechnology becomes possible when knowing which microbes compose the community, how and when they interact to each other, and what are the outcomes of their biochemical communication. Using the attine ant fungus garden as example, samples from insect fungiculture environment could compose the initial inoculum for degradation assays, performed through interconnected (A) culture-dependent and (B) culture-independent workflows. This would allow invetigating the metabolic potential of the associated microbiota without threatening insect populations. Pencil drawing illustrations by Mariana Barcoto. PCA and heatmap were set up using random annotations, and do not comprise actual data.