Impact of Mixed Infections of Gut Parasites Lotmaria passim and Nosema ceranae on the Lifespan and Immune-related Biomarkers in Apis mellifera

Abstract

<jats:p>Lotmaria passim currently appears to be the predominant trypanosome in honey bees worldwide. Although, the specific effects of L. passim by single or mixed with other gut parasites such as Nosema ceranae on honey bees’ health is still unclear. We consequently measured bees’ survival, parasite loads, the expression of antimicrobial peptides (AMPs) and vitellogenin gene. Thus, (1) bees naturally infected with L. passim, (2) healthy bees inoculated with Nosema ceranae, (3) bees naturally infected with L. passim and inoculated with N. ceranae and (4) healthy bees (control) were maintained under controlled conditions. Honey bees infected with N. ceranae or with mixed infections of L. passim and N. ceranae had significantly lower survival rates than the control group at 20 days post-inoculation (dpi). A competitive suppression was also detected, provided that the L. passim load was significantly affected by the presence of N. ceranae at 15 dpi. Expressions of the AMPs defensin and hymenoptaecin rapidly (two hours post-inoculation) increased in bees infected with N. ceranae and mixed infections. However, this effect was not continuous. In fact, expressions of abaecin, defensin, hymenoptaecin and vitellogenin decreased drastically at 15 dpi in bees with both single and mixed infections. The decrease in the expression of AMPs and vitellogenin throughout this period was consistent with the reduced survivals observed in this study, indicating that mixed infections of L. passim and N. ceranae, and even into a scenario of competition between them, may have a synergic effect on the survival and immune-related gene expressions (biomarkers) of worker bees.</jats:p>

Workflow of Lotmaria passim isolation: Experimental infection with a low-passage strain causes higher honeybee mortality rates than the PRA-403 reference strain

“…One such study reported an almost identical mortality rate following mixed C. mellificae and N. ceranae infections to that produced by single microsporidian infection ( Higes et al, 2016 ). However, a recent study of naturally infected L. passim bees inoculated with N. ceranae reported higher mortality than that in the individual infection by each organism alone ( Arismendi et al, 2020b ). Thus, to remove any potential effect on bee mortality rates, those infected with N. ceranae were removed from the mortality study.…”

Pathogens Spillover from Honey Bees to Other Arthropods

“…Transmission route and impact on bees are very similar to the other parasite L. passim [ 187 , 188 , 192 ]. C. mellificae was almost completely replaced by L. passim and its infection has been rarely observed [ 185 , 193 , 194 ].…”

Detection of Lotmaria passim, Crithidia mellificae and Replicative Forms of Deformed Wing Virus and Kashmir Bee Virus in the Small Hive Beetle (Aethina tumida)

“…To date, only a few instances of individual SHBs bearing bee pathogens have been reported. This is the case for samples from Mexico (positive for L. passim , Apis mellifera filamentous virus (AmFV), C. bombi , Ascosphera apis , and Nosema ceranae [ 22 ]), Florida (positive for N. ceranae [ 20 ]), and other areas of the USA (positive for DWV, SBV and P. larvae [ 19 , 20 , 22 , 24 ]).…”

“…Lotmaria passim and Crithidia mellificae are two trypanosomatid species capable of colonizing the digestive system of honey bees [ 24 , 25 ]. The transmission is deemed to occur by the oral–fecal route [ 26 , 27 ], and the presence of infected faeces within the hive may promote the circulation of the parasite among worker bees [ 26 ].…”