First description of Lotmaria passim and Crithidia mellificae haptomonad stages in the honeybee hindgut

Buendía-Abad, María; García-Palencia, Pilar; Pablos, Luis Miguel De; Alunda, José María; Osuna, Antonio; Martín-Hernández, Raquel; Higes, Mariano

doi:10.1016/j.ijpara.2021.06.005

Cited by 17 publications

(25 citation statements)

References 64 publications

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“…The C. acanthocephali reference strain (ATCC 30251, American Type Culture Collection) was cultured in vitro to generate the inoculum, establishing serial cultures to infect honey bees with trypanosomatids at the same developmental stage on consecutive days. Starting from an initial concentration of 10 5 cells/mL, the cells were cultured as described previously for C. mellificae and L. passim [13], maintaining them at 27 • C in 25 cm 2 flasks (Corning, New York, NY, USA) in Brain Heart Infusion broth (BHI; Sigma-Aldrich, Merck KGaA, Darmstadt, Germany) supplemented with 10% heat-inactivated fetal bovine serum (HIFBS, Gibco, Thermo-Fisher Scientific, Waltham, MA, USA) and 1% penicillin/streptomycin (Lonza, Basel, Switzerland) [13]. After 96-168 h, the cultures had reached the early stationary phase, and the choanomastigote forms of C. acanthocephali were obtained to be used as an inoculum [13].…”

Section: Methodsmentioning

confidence: 99%

“…Starting from an initial concentration of 10 5 cells/mL, the cells were cultured as described previously for C. mellificae and L. passim [13], maintaining them at 27 • C in 25 cm 2 flasks (Corning, New York, NY, USA) in Brain Heart Infusion broth (BHI; Sigma-Aldrich, Merck KGaA, Darmstadt, Germany) supplemented with 10% heat-inactivated fetal bovine serum (HIFBS, Gibco, Thermo-Fisher Scientific, Waltham, MA, USA) and 1% penicillin/streptomycin (Lonza, Basel, Switzerland) [13]. After 96-168 h, the cultures had reached the early stationary phase, and the choanomastigote forms of C. acanthocephali were obtained to be used as an inoculum [13]. The cells were counted in a Neubauer chamber and the inoculum concentration was adjusted with Phosphate Buffered Saline (PBS) to 5 × 10 4 cells/µL.…”

Section: Methodsmentioning

confidence: 99%

“…Both L. passim and C. mellificae have been recently found to modify their promastigote and choanomastigote morphology into an haptomonad form, remodeling their flagella into an attachment pad that allows them to remain attached to the gut walls of their host and cover the epithelial cells [13]. This haptomonad stage and its morphogenesis have been described in other trypanosomatid species, such as Leishmania, and it is regarded as an influential factor for parasite survival and transmission [14][15][16].…”

Section: Introductionmentioning

confidence: 99%

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The Haptomonad Stage of Crithidia acanthocephali in Apis mellifera Hindgut

Buendía-Abad

García-Palencia

Pablos

et al. 2022

Veterinary Sciences

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Crithidia acanthocephali is a trypanosomatid species that was initially described in the digestive tract of Hemiptera. However, this parasite was recently detected in honey bee colonies in Spain, raising the question as to whether bees can act as true hosts for this species. To address this issue, worker bees were experimentally infected with choanomastigotes from the early stationary growth phase and after 12 days, their hindgut was extracted for analysis by light microscopy and TEM. Although no cellular lesions were observed in the honey bee’s tissue, trypanosomatids had differentiated and adopted a haptomonad morphology, transforming their flagella into an attachment pad. This structure allows the protozoa to remain attached to the gut walls via hemidesmosomes-such as junctions. The impact of this species on honey bee health, as well as the pathogenic mechanisms involved, remains unknown. Nevertheless, these results suggest that insect trypanosomatids may have a broader range of hosts than initially thought.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The Haptomonad Stage of Crithidia acanthocephali in Apis mellifera Hindgut

Buendía-Abad

García-Palencia

Pablos

et al. 2022

Veterinary Sciences

Self Cite

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“…Insect-infecting trypanosomatids have generally been considered benign; however, more recently, they have been implicated as pathogens that have negative impacts on pollinator health, particularly species within the genera Crithidia and Lotmaria [ 100 , 101 ]. It is unclear how these organisms cause pathogenic effects in their hosts, but one hypothesis is that they may carpet the hindgut, obstructing absorption or sequestering nutrients, resulting in a nutritional deficit for the host [ 102 ]. Crithidia species have not been identified as causing disease in commercially reared insects; however, they are increasingly reported to have low host specificity, not only infecting a broad range of insects but also multiple mammalian species [ 103 ].…”

Section: Protist Parasites Including Microsporidia Within the Eu Rear...mentioning

confidence: 99%

Protists in the Insect Rearing Industry: Benign Passengers or Potential Risk?

Bessette

Williams

2022

Insects

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As the insects for food and feed industry grows, a new understanding of the industrially reared insect microbiome is needed to better comprehend the role that it plays in both maintaining insect health and generating disease. While many microbiome projects focus on bacteria, fungi or viruses, protists (including microsporidia) can also make up an important part of these assemblages. Past experiences with intensive invertebrate rearing indicate that these parasites, whilst often benign, can rapidly sweep through populations, causing extensive damage. Here, we review the diversity of microsporidia and protist species that are found in reared insect hosts and describe the current understanding of their host spectra, life cycles and the nature of their interactions with hosts. Major entomopathogenic parasite groups with the potential to infect insects currently being reared for food and feed include the Amoebozoa, Apicomplexa, Ciliates, Chlorophyta, Euglenozoa, Ichtyosporea and Microsporidia. However, key gaps exist in the understanding of how many of these entomopathogens affect host biology. In addition, for many of them, there are very limited or even no molecular data, preventing the implementation of molecular detection methods. There is now a pressing need to develop and use novel molecular tools, coupled with standard molecular diagnostic methods, to help unlock their biology and predict the effects of these poorly studied protist parasites in intensive insect rearing systems.

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“…Environmental pollutants such as agrochemicals [4][5][6] and heavy metals [7,8], together with pathogens [9,10], inadequate fl oral resources [11,12] and incorrect beekeeping practices [2] have been accused of having contributed to the decline in the number of bees. Among pathogens, there are endoparasites capable of compromising bee health and contribute to colony mortality, like microsporidia [13][14][15][16][17] and trypanosomatids [18][19][20], but also viruses [21][22][23][24][25]. However, they do not necessarily infl ict damage per se, but may synergistically infl uence bees and even lead to colony death [26][27][28][29][30].…”

Section: Introductionmentioning

confidence: 99%

Diet Supplementation Helps Honey Bee Colonies in Combat Infections by Enhancing their Hygienic Behaviour

et al. 2022

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The hygienic behavior in honey bees is a complex polygenic trait that serves as a natural defense mechanism against bacterial and fungal brood diseases and Varroa destructor mites infesting brood cells. The aim of this study was to evaluate the effect of a dietary amino acids and vitamins supplement “BEEWELL AminoPlus” on hygienic behavior of Apis mellifera colonies combating microsporidial and viral infections. The experiment was performed during a one-year period on 40 colonies alloted to five groups: one supplemented and infected with Nosema ceranae and four viruses (Deformed wing virus - DWV, Acute bee paralysis virus - ABPV, Chronic bee paralysis virus - CBPV and Sacbrood virus – SBV), three not supplemented, but infected with N. ceranae and/ or viruses, and one negative control group. Beside the l isted pathogens, honey bee trypanosomatids were also monitored in all groups. The supplement “BEEWELL AminoPlus” induced a significant and consistent increase of the hygienic behavior in spite of the negative effects of N. ceranae and viral infections. N. ceranae and viruses significantly and consistently decreased hygienic behavior, but also threatened the survival of bee colonies. The tested supplement showed anti-Nosema effect, since the N. ceranae infection level significantly and consistently declined only in the supplemented group. Among infected groups, only the supplemented one remained Lotmaria passim-free throughout the study. In conclusion, diet supplementation enhances hygienic behavior of honey bee colonies and helps them fight the most common infections of honey bees.

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First description of Lotmaria passim and Crithidia mellificae haptomonad stages in the honeybee hindgut

Cited by 17 publications

References 64 publications

The Haptomonad Stage of Crithidia acanthocephali in Apis mellifera Hindgut

The Haptomonad Stage of Crithidia acanthocephali in Apis mellifera Hindgut

Protists in the Insect Rearing Industry: Benign Passengers or Potential Risk?

Diet Supplementation Helps Honey Bee Colonies in Combat Infections by Enhancing their Hygienic Behaviour

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