Temperature dependence of parasitic infection and gut bacterial communities in bumble bees

Abstract

Summary High temperatures (e.g., fever) and gut microbiota can both influence host resistance to infection. However, effects of temperature‐driven changes in gut microbiota on resistance to parasites remain unexplored. We examined the temperature dependence of infection and gut bacterial communities in bumble bees infected with the trypanosomatid parasite Crithidia bombi. Infection intensity decreased by over 80% between 21 and 37°C. Temperatures of peak infection were lower than predicted based on parasite growth in vitro, consistent with mismatches in thermal performance curves of hosts, parasites and gut symbionts. Gut bacterial community size and composition exhibited slight but significant, non‐linear, and taxon‐specific responses to temperature. Abundance of total gut bacteria and of Orbaceae, both negatively correlated with infection in previous studies, were positively correlated with infection here. Prevalence of the bee pathogen‐containing family Enterobacteriaceae declined with temperature, suggesting that high temperature may confer protection against diverse gut pathogens. Our results indicate that resistance to infection reflects not only the temperature dependence of host and parasite performance, but also temperature‐dependent activity of gut bacteria. The thermal ecology of gut parasite‐symbiont interactions may be broadly relevant to infectious disease, both in ectothermic organisms that inhabit changing climates, and in endotherms that exhibit fever‐based immunity.

Cross-infectivity of honey and bumble bee-associated parasites across three bee families

“…The cell suspension was then mixed with an equal quantity of 4 m m ( C. mellificae ) or 16 m m ( L. passim and C. bombi ) aqueous sucralose (trade name ‘Splenda’, Heartland Food Products, UK) water for a final concentration of 1000 parasites μ L −1 . The sucralose solution was used to provide a sweet taste that encouraged consumption without the osmotic stress of a high-sugar solution (Palmer-Young et al ., 2019 a , 2019 b ), which can kill trypanosomatid cells (Cisarovsky and Schmid-Hempel, 2014); we observed that cells rapidly became deformed and immotile in 50% sugar water. The higher 16 m m sucralose concentration (8 m m in final inoculum) was used in the final 2 weeks of the experiment after this concentration was found to promote consumption.…”

“…Bombus impatiens and A. mellifera are both corbiculate (‘pollen-basket’) bees within the family Apidae, and both harbour a socially transmitted, phylogenetically similar gut microbiota (Kwong et al ., 2017) that is a key mediator of trypanosomatid infection in the Bombus spp./ Crithidia spp. system (Koch and Schmid-Hempel, 2011, 2012; Mockler et al ., 2018; Palmer-Young et al ., 2019 a , 2019 b ). In contrast, solitary bees – as well as the facultatively eusocial Halictids – lack the socially transmitted core gut microbiota that is a feature of B. impatiens and A. mellifera (McFrederick et al ., 2012, 2014, 2016; Kwong et al ., 2017).…”

“…However, 30°C conditions for A. mellifera adults have been used successfully by other authors (Forsgren and Fries, 2010; Williams et al ., 2013), and future cross-infection experiments should ideally apply the same temperature conditions for all hosts. For example, the 28–32°C temperature range is ideal for growth of C. bombi , whereas higher temperatures inhibited in vitro parasite growth, potentiated the antagonistic effects of gut symbionts (Palmer-Young et al ., 2018 b ), and reduced infection prevalence and intensity in B. impatiens (Palmer-Young et al ., 2019 a , 2019 b ). The only study to date that found temporary persistence of C. bombi in A. mellifera used a lower rearing temperature of 30°C (Ruiz-González and Brown, 2006), which is within the range of peak C. bombi growth rate in vitro (Palmer-Young et al ., 2018 b ) and allowed substantial infection in B. impatiens (Palmer-Young et al ., 2019 a , 2019 b ).…”

“…bees allow maintenance of consistently high nest temperatures (Esch, 1960; Heinrich, 1972, 1974) that could constrain establishment of environmental microbes (Casadevall, 2016), the relatively low and variable temperatures experienced by small solitary bees in the wild could increase their susceptibility to trypanosomatid infection. Studies of these and additional host species could discern the importance of physiochemical properties of the gut lumen – such as microbiota, pH, temperature and pollen type and availability (Koch and Schmid-Hempel, 2011; Conroy et al ., 2016; Giacomini et al ., 2018; Palmer-Young et al ., 2018 b , 2019 a , 2019 b ) – for establishment of infection.…”

“…Three strains of C. bombi were isolated from infected wild bumble bees ( B. impatiens and B. terrestris ) by single cell sorting: strains ‘12.6’ (from B. impatiens in Lufkin, TX in 2014 by Hauke Koch), ‘IL13.2’ (from B. impatiens in Normal, IL in 2013 by Ben Sadd) and ‘C1.1’ (from B. terrestris in Corsica, France in 2012 by Ben Sadd) (Palmer-Young et al ., 2016). Species identity was confirmed by sequencing of the GAPDH gene (Palmer-Young et al ., 2019 a , 2019 b ). Parasites were grown at 27°C in vented culture flasks with modified Mattei growth medium as previously described (Salathé et al ., 2012).…”