Seasonal shifts in the insect gut microbiome are concurrent with changes in cold tolerance and immunity

Abstract

Seasonal changes in the environment, such as varying temperature, have the potential to change the functional relationship between ectothermic animals, such as insects, and their microbiomes. Our objectives were to determine: (a) whether seasonal changes in temperature shift the composition of the insect gut microbiome, and (b) whether changes in the microbiome are concomitant with changes in the physiology of the host, including the immune system and response to cold. We exposed laboratory populations of the spring field cricket, Gryllus veletis (Orthoptera: Gryllidae), to simulated overwintering conditions in both a laboratory microcosm and a field‐like microcosm containing soil and leaves. In summer, autumn, winter and spring, we extracted and sequenced 16S bacterial genomic DNA from cricket guts, to capture seasonal variation in the composition of the microbiome. The composition of the gut microbiome was similar between microcosms, and overall highly anaerobic. In both microcosms, we captured similar seasonal variation in the composition of the microbiome, where overwintering resulted in permanent changes to these microbial communities. In particular, the abundance of Pseudomonas spp. decreased, and that of Wolbachia spp. increased, during overwintering. Concurrent with overwintering changes in the gut microbiome, G. veletis acquire freeze tolerance and immune function shifts temporarily, returning to summer levels of activity in the spring. In a specific manner, haemocyte concentrations increase but survival of fungal infection decreases in the winter, whereas the ability to clear bacteria from the haemolymph remains unchanged. Overall, we demonstrate that the gut microbiome does shift seasonally, and in concert with other physiological changes. We hypothesize that these changes may be linked, and suggest that it will next be important to determine whether these changes in the microbiome contribute to host overwintering success. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13153/suppinfo is available for this article.

Transgenerational inheritance of cold temperature response in Drosophila

“…This supported the original indirect evidence on fecal transfer that paternally acquired bacteria contribute to transcriptional responses observed in the offspring of cold‐exposed fathers . The contribution of acquired microbiota in offspring transcriptional responses seems consistent with previous studies showing an influence of gut microbiota on thermal phenotype and a correlation of gut microbiome load with cold tolerance in D. melanogaster as well as an association between the gut microbiota composition and host physiology in cold tolerance in the field cricket Gryllus veletis . Indeed, emerging evidence increasingly support, across species, microbiome–germline interaction and bacteria‐mediated transgenerational inheritance .…”

Abdominal microbial communities in ants depend on colony membership rather than caste and are linked to colony productivity

“…This suggests that laboratory conditions do not necessarily lead to a decrease in bacterial community diversity between and within colonies in T. nylanderi but that rather seasonality might be responsible for more similar communities among T. nylanderi ants. Seasonal cycles were described for mammals, including humans (e.g., Maurice et al, ; Smits et al, ), but there is little information on seasonality in bacterial communities in wild insect populations (but see Ferguson et al, ).…”

Metacommunity theory for transmission of heritable symbionts within insect communities

“…In some cases, insects have lost their endosymbionts completely following sufficiently strong heat-shock events (Thomas & Blanford, 2003). The sensitivity of bacterial symbionts to temperature suggests that the benefits and costs provided to hosts could be substantially altered in scenarios of significant environmental (Ross et al, 2017) and seasonal (Ferguson et al, 2018) change. These responses require further investigation, especially in the context of changing temperatures predicted to cause increased abiotic stress (Corbin et al, 2017).…”