Nosema spp. infections cause no energetic stress in tolerant honeybees

Abstract

Host-pathogen coevolution leads to reciprocal adaptations, allowing pathogens to increase host exploitation or hosts to minimise costs of infection. As pathogen resistance is often associated with considerable costs, tolerance may be an evolutionary alternative. Here, we examined the effect of two closely related and highly host dependent intracellular gut pathogens, Nosema apis and Nosema ceranae, on the energetic state in Nosema tolerant and sensitive honeybees facing the infection. We quantified the three major haemolymph carbohydrates fructose, glucose, and trehalose using high-performance liquid chromatography (HPLC) as a measure for host energetic state. Trehalose levels in the haemolymph were negatively associated with N. apis infection intensity and with N. ceranae infection regardless of the infection intensity in sensitive honeybees. Nevertheless, there was no such association in Nosema spp. infected tolerant honeybees. These findings suggest that energy availability in tolerant honeybees was not compromised by the infection. This result obtained at the individual level may also have implications at the colony level where workers in spite of a Nosema infection can still perform as well as healthy bees, maintaining colony efficiency and productivity.

Infection dynamics of Nosema ceranae in honey bee midgut and host cell apoptosis

“…Interestingly, Huang et al (2012) showed a higher survival and increased immune responses in those tolerant bees compared to sensitive bees from an unselected lineage, despite suffering similar infection intensities of N. ceranae. In subsequent experiments, infected worker bees from this Nosema tolerant linage appeared to neither experience decreased rates of apoptosis (one form of PCD) (Kurze et al, 2015) nor energetic stress (Kurze et al, 2016b). A similar pattern was also found when comparing the midgut proteomes between infected workers of both the Nosema tolerant and a Nosema sensitive lineage (Kurze et al, 2016a).…”

“…A breeding program selecting against Nosema over 20 years resulted in a Nosema tolerant honey bee lineage (Hatjina et al, 2014). Although Nosema prevalence reduced from 60-80% down to about 10% in selected colonies (Hatjina et al, 2014), individual bees were still susceptible to both Nosema apis and N. ceranae in laboratory experiments (Kurze et al, 2016b). Interestingly, Huang et al (2012) showed a higher survival and increased immune responses in those tolerant bees compared to sensitive bees from an unselected lineage, despite suffering similar infection intensities of N. ceranae.…”

“…Nosema is primarily transmitted via the fecal-oral route between adult bees and establishes an infection in the midgut epithelium (Fries, 2010). Over the course of infection, N. ceranae has been shown to induce multiple physiological alterations in its host, including processes involved in the regulation of programmed cell death (PCD) (Doublet et al, 2017;Higes et al, 2013a;Kurze et al, 2015;Martin-Hernandez et al, 2017) and energy metabolism (Kurze et al, 2016b;Mayack and Naug, 2009;Vidau et al, 2014). This might be not surprising as microsporidia rely on their host metabolism for supply of energy resources (Keeling, 2009).…”

Disruption of oxidative balance in the gut of the western honeybee Apis mellifera exposed to the intracellular parasite Nosema ceranae and to the insecticide fipronil

“…Several studies revealed differences in honeybee susceptibility to infection by N. ceranae . Such differences may result from resistance or tolerance mechanisms mediated by the genetic variability of honeybees (Fontbonne et al ., ; Kurze et al ., ,b) but could also be due to life‐history traits of bee colonies used in the different studies. Indeed, sampled bees used for experimental studies may have been impacted in their colony by multiple factors including resources, contaminants or pathogens.…”

Nosema ceranae in Apis mellifera: a 12 years postdetection perspective

“…The alterations of the carbohydrate metabolism reflect the nutritional and energetic stress experienced by N. ceranae infected honey bees (Mayack and Naug, 2010;Aliferis et al, 2012;Vidau et al, 2014). Interestingly, this has not been observed in Nosema tolerant honey bees (Kurze et al, 2016). Energetic stress has been described in infected foragers that were hungrier than uninfected bees (Mayack and Naug, 2009), consuming more sugar Martín-Hern andez et al, 2011;Vidau et al, 2011).…”