Reduced environmental microbial diversity on the cuticle and in the galleries of a subterranean termite compared to surrounding soil

Authors: AGUERO, CARLOS - Texas A&M University; EYER, PIERRE-ANDRÉ - Texas A&M University; Crippen, Tawni - Tc; VARGO, EDWARD - Texas A&M University

Submitted to: Microbial Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/9/2020
Publication Date: 1/5/2021
Citation: Aguero, C.M., Eyer, P., Crippen, T.L., Vargo, E.L. 2021. Reduced environmental microbial diversity on the cuticle and in the galleries of a subterranean termite compared to surrounding soil. Microbial Ecology. 81(4):1054-1063. https://doi.org/10.1007/s00248-020-01664-w.
DOI: https://doi.org/10.1007/s00248-020-01664-w

Interpretive Summary: Termites are a pest commonly found in the Southern United States affecting structures at animal production facilities. Very little is known about their microbiome and the commensal and pathogenic organisms they carry. This study characterizes the bacterial and fungal communities on the cuticle of the termite, as well as in the tunnels/pathways (foraging galleries) constructed by the termites and the surrounding soil to determine the microbial populations present. The termite foraging galleries are made from a mixture of soil, termite saliva, and feces. Interestingly, when examining the foraging galleries, they harbored many beneficial microbes, including Streptomyces and methane-utilizing bacterial groups (methanotrophs). However, these subterranean termites also had several pathogens on their cuticle (e.g. Serratia, Pseudomonas, and Aspergillus sp.). Serratia sp. is similar in structure to Escherichia coli and Klebsiella sp. and can be an opportunistic gram-negative pathogen responsible for infections, such as mastitis in dairy cattle; and along with Pseudomonas sp., can be involved in food spoilage, such as contaminated milk or meat. Some Aspergillus sp., a mold, can cause respiratory illnesses (Aspergillosis) in most animals and mastitis in cattle.

Technical Abstract: Termites are intimately tied to the microbial world, as they utilize their gut microbiome for the conversion of plant cellulose into necessary nutrients. Subterranean termites must also protect themselves from the vast diversity of harmful microbes found in soil. However, not all soil microbes are harmful, such as Streptomyces and methanotrophic bacteria that some species of termites harbor in complex nest structures made of fecal material. The eastern subterranean termite, Reticulitermes flavipes, has a simple nest structure consisting of fecal lined galleries. We tested the hypothesis that R. flavipes maintains a select microbial community in its nests to limit the penetration of harmful soilborne pathogens and favor the growth of beneficial microbes. Using Illumina sequencing, we characterized the bacterial and fungal communities in the surrounding soil, in the nest galleries, and on the cuticle of workers. We found that the galleries provide a more beneficial microbial community than the surrounding soil. Bacterial and fungal diversity was highest in the soil, lower in the galleries, and least on the cuticle. Bacterial communities clustered together according to the substrate from which they were sampled, but this clustering was less clear in fungal communities. Most of the identified bacterial and fungal taxa were unique to one substrate, but the soil and gallery communities had very similar phylum-level taxonomic profiles. Notably, the galleries of R. flavipes also harbored both the potentially beneficial Streptomyces and the methanotrophic Methylacidiphilales, indicating that these microbial associations in fecal material pre-date the emergence of complex fecal nest structures. Surprisingly, several pathogenic groups were relatively abundant in the galleries and on the cuticle, suggesting that pathogens may accumulate within termite nests over time while putatively remaining at enzootic level during the lifetime of the colony.