The peritrophic matrix delays Nosema ceranae infection in the honey bee Apis mellifera midgut

Abstract

The midgut of bees plays a significant role in digestion and absorption and is a gateway for pathogens. As a protection for the organism, the midgut lumen is lined by a peritrophic matrix rich in chitin fibrils, associated with proteins that form multiple resistant layers with gelatinous consistency, with several functions, including the mechanical barrier against infection by pathogens. The obligate intracellular microsporid Nosema ceranae is an important pathogen that decreases honey production, increases pesticide susceptibility, and may cause mortality in the honey bee Apis mellifera. This study evaluated whether the peritrophic matrix has a protective function against infection by N. ceranae in A. mellifera adult workers. The peritrophic matrix integrity was changed by feeding the bees with calcofluor white (CFW), followed by an artificial infection with N. ceranae spores. Results shown that 0.5% CFW affect the integrity of the peritrophic matrix with areas of interruption of this envelope. This disorganization of the peritrophic matrix reduces the life cycle period of N. ceranae from eight to four days, after inoculation, and increases the concentration of new spores released in the midgut lumen. This is the first report on the importance of the peritrophic matrix as a protective barrier against N. ceranae infection in A. mellifera.

Influence of Age of Infection on the Gut Microbiota in Worker Honey Bees (Apis mellifera iberiensis) Experimentally Infected with Nosema ceranae

“…This positive association between G. apicola and experimental N. ceranae infection seems to be very common, as it was found by other authors [56,58,[62][63][64] in trials conducted under very different conditions, addressing infection at different ages, different honey bee subspecies, distinct spore doses, gut regions examined, diets fed, analytical methods, or through the analysis of individual bees or pooled samples. However, others failed to find any association between N. ceranae infection and this bacterium or with any other bacteria [65], while other studies found associations with other bacteria like those of the genera Lactobacillus, Bifidobacterium, Snodgrassella, or Bartonella [61,62,[66][67][68][69], which did not appear to be modified here. Most of these studies used very young bees (24-48 h p.e.)…”

“…were much more susceptible to N. ceranae infection. This may be because newly emerged bees do not have well-developed peritrophic membranes [68] and the absence of this physical barrier may favour the infection of midgut epithelial cells. Although there were no significant differences in the 8-day-old bees studied here, this trend was similar to that on the previous day.…”

Efeitos histopatológicos do inseticida teflubenzurom no intestino médio de operárias da abelha Apis mellifera (Hymenoptera: Apidae)

“…O intestino médio dos insetos é a porta de entrada de nutrientes e compostos químicos Em A. mellifera, o intestino médio é caracterizado por um epitélio simples, com células colunares digestivas com microvilosidades na superfície apical e núcleo esférico, sendo a principal seção do trato digestório com função de secreção de enzimas digestivas e absorção de nutrientes e o lúmen é revestido por camadas acelulares semipermeáveis que formam a matriz peritrófica, sendo mais espessa na região posterior em relação à anterior do intestino médio (Oliveira e al., 2019;Castro et al, 2020;Serra et al, 2021;Carneiro et al, 2022). A matriz peritrófica é composta por fibrilas de quitina, glicosaminoglicanos, glicoproteínas e proteínas, sintetizadas pelas células do intestino médio (Hegedus et al, 2009;Liu et al, 2019) com função de proteger o epitélio contra abrasão mecânica (Hegedus et al, 2009), prevenção de infecções por microorganismos (Lahane, 1997;Kuraishi et al, 2011;Sadlova et al, 2018;Erlandson et al, 2019;Oliveira et al, 2022), toxinas e outras substâncias danosas (Guo et al, 2019), além de promover o aumento da eficiência da digestão (Bolognesi, 2008).…”