Thermal niches of specialized gut symbionts: the case of social bees

Abstract

1 2 Responses to climate change are particularly complicated in species that engage in 3 symbioses, as the niche of one partner may be modified by that of the other. We explored 4 thermal traits in gut symbionts of honeybees and bumblebees, which are vulnerable to rising 5 temperatures. In vitro assays of symbiont strains isolated from 16 host species revealed variation 6 in thermal niches. Strains from bumblebees tended to be less heat-tolerant than those from 7 honeybees, possibly due to bumblebees maintaining cooler nests or inhabiting cooler climates. 8Overall however, bee symbionts grew at temperatures up to 44 °C and withstood temperatures up 9 to 52 °C, at or above the upper thermal limits of their hosts. While heat-tolerant, most strains of 10 the symbiont Snodgrassella grew relatively slowly below 35 °C, perhaps because of adaptation 11 to the elevated body temperatures that bees maintain through thermoregulation. In a gnotobiotic 12 bumblebee experiment, Snodgrassella was unable to consistently colonize bees reared below 35 13 °C under conditions that limit thermoregulation. Thus, host thermoregulatory behavior appears 14 important in creating a warm microenvironment for symbiont establishment. Bee-microbiome-15 temperature interactions could affect host health and pollination services, and inform research on 16 the thermal biology of other specialized gut symbionts, such as those of humans. 17 18 19 20 Earth's climate is rapidly warming, and there is an urgent need to understand how 21 organisms will respond [1,2]. One factor complicating such predictions is the role of interspecific 22 interactions [3,4], and, in particular, symbiosis [5,6]. Many organisms closely associate with one 23 or more distantly related partners that have highly distinct physiologies, as in the case of animal 24 or plant hosts and their microbiomes. Hosts and microbes are likely to have different responses 25 to temperature; yet, if they are mutually dependent, the combined niche is restricted to that of the 26 more sensitive partner. Furthermore, thermal niches can themselves evolve in response to 27 symbiotic lifestyles. For example, obligate endosymbionts that undergo strong population 28 bottlenecks during transmission may evolve unstable, easily denatured proteins as a consequence 29 of mutation accumulation, leading to heat sensitivity [7][8][9]. Both of these factors may constrain 30 the combined thermal niche of strongly symbiont-dependent organisms [6,10,11]. There is 31 evidence for symbiont-imposed constraints on host thermotolerance in a variety of invertebrates 32 such as aphids, ants, stinkbugs, corals, and sponges [12][13][14][15][16]. However, the wider prevalence of 33 this phenomenon is unclear, and, in general, we do not know how microbiomes will influence 34 host responses to climate warming. 35The eusocial corbiculate bees (hereafter "social bees") are a particularly important group 36 in which to study symbiont thermal niches and their effects on hosts. This clade, comprising 37 honey bees (Apis), bumb...

Microbiome assembly and maintenance across the lifespan of bumble bee workers

“…Amounts of bacterial DNA in newly emerged adult guts are very low (Fig. 1A), and previous work finding these guts generally devoid of culturable bacteria (77, 78) suggests that this DNA may derive from nonviable cells. Larvae harbor Lactobacillus and Apilactobacillus (Fig.…”

“…One is an interaction between host and symbiont genotypes (77). There may also be genotype-by-environment effects; to give one example, bee colonies of different sizes may have different thermoregulatory capacities and temperatures (87); this could act as an ecological filter for strains with different thermal tolerances (78). In addition to intrinsic physiological differences between strains, differences in temperature or other environmental factors may explain why the inferred replication rates of Schmidhempelia differed substantially between colonies (Fig.…”

Prospects for probiotics in social bees

“…For example, the gut community composition is drastically affected by exposure to antibiotics [29,49] or to some herbicides [28,30,50]. Bee gut communities can be impacted by diet, including nutrient quantity, nutrient composition and phytochemicals present in nectar, pollen and propolis [51], and by temperature [52,53]. In honeybees, perturbed gut communities are more susceptible to invasion by pathogens, as observed in challenge experiments with S. marcescens [28] and Nosema [10,54] .…”

Bumblebees with the socially transmitted microbiome: A novel model organism for gut microbiota research

“…Although the gut bacteria from Bombus and Apis are host‐specialized, Bombus species and subgenera often share closely related symbionts (Koch et al ., 2013). For example, Snodgrassella strains isolated from 1 Bombus species can robustly colonize the gut of other Bombus species (Kwong et al ., 2014; Hammer et al ., 2021a).…”