Life cycle of Blastocrithidia papi sp. n. (Kinetoplastea, Trypanosomatidae) in Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae)

Frolov, Andrei N.; Malysheva, Marina N.; Ganyukova, Anna I.; Yurchenko, Vyacheslav; Kostygov, Alexei Y.

doi:10.1016/j.ejop.2016.10.007

Cited by 22 publications

(26 citation statements)

References 64 publications

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“…In D. fasciatus , the occurrence of bacterial symbionts on the peritrophic matrix lining the gut wall is the most likely explanation for differences in the observed parasite titres. Trypanosomatids are known to colonize the guts of insects by adhering to the midgut peritrophic matrix (Frolov et al., ; Hamilton, Votypka, et al., ; Maslov et al., ; Romeiro et al., ). In fact, mutations in the major component of this matrix, drosocrystallin, increase the severity of infections with the entomopathogenic bacterium Pseudomonas entomophila, and the trypanosomatid parasite Jaenimonas drosophilae in Drosophila (Hamilton, Votypka, et al., ; Kuraishi, Binggeli, Opota, Buchon, & Lemaitre, ), and knockdown of PpPer1, a molecular component of the peritrophic matrix in the sand‐fly Phlebotomus papatasi, results in higher Leishmania infection loads (Coutinho‐Abreu, Sharma, Robles‐Murguia, & Ramalho‐Ortigao, ).…”

Section: Discussionmentioning

confidence: 99%

The cotton stainer's gut microbiota suppresses infection of a cotransmitted trypanosomatid parasite

2018

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The evolutionary and ecological success of many insects is attributed to mutualistic partnerships with bacteria that confer hosts with novel traits including food digestion, nutrient supplementation, detoxification of harmful compounds and defence against natural enemies. Dysdercus fasciatus firebugs (Hemiptera: Pyrrhocoridae), commonly known as cotton stainers, possess a simple but distinctive gut bacterial community including B vitamin-supplementing Coriobacteriaceae symbionts. In addition, their guts are often infested with the intestinal trypanosomatid parasite Leptomonas pyrrhocoris (Kinetoplastida: Trypanosomatidae). In this study, using experimental bioassays and fluorescence in situ hybridization (FISH), we report on the protective role of the D. fasciatus gut bacteria against L. pyrrhocoris. We artificially infected 2nd instars of dysbiotic and symbiotic insects with a parasite culture and measured parasite titres, developmental time and survival rates. Our results show that L. pyrrhocoris infection increases developmental time and slightly modifies the quantitative composition of the gut microbiota. More importantly, we found significantly higher parasite titres and a tendency towards lower survival rates in parasite-infected dysbiotic insects compared to symbiotic controls, indicating that the gut bacteria successfully interfere with the establishment or proliferation of L. pyrrhocoris. The colonization of symbiotic bacteria on the peritrophic matrix along the gut wall, as revealed by FISH, likely acts as a barrier blocking parasite attachment or entry into the hemolymph. Our findings show that in addition to being nutritionally important, D. fasciatus' gut bacteria complement the host's immune system in preventing parasite invasions and that a stable gut microbial community is integral for the host's health.

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Section: Discussionmentioning

confidence: 99%

The cotton stainer's gut microbiota suppresses infection of a cotransmitted trypanosomatid parasite

2018

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“…These flagellates are distinct from others in their ability to form a specialized resting stage–cyst-like amastigotes (CLAs), adapted to long-term survival in the environment [ 12 – 14 ]. All species of this group known to date were described from true bugs (order Hemiptera) [ 2 , 11 , 15 , 16 ]. The CLAs can survive outside the host for over 10 years in laboratory conditions and are able to withstand both low and high temperatures (from that of liquid nitrogen to + 60°C), treatment with detergents and desiccation [ 17 – 20 ].…”

Section: Introductionmentioning

confidence: 99%

“…However, there are some exceptions: Blastocrithidia triatomae parasitizing triatomine bugs, Leptomonas wallacei from the lygaeid bug Oncopeltus fasciatus , and B . papi from the firebug Pyrrhocoris apterus [ 12 , 15 , 31 ]. Blastocrithidia triatomae was extensively studied because of its pathogenic effect on the insect hosts, which transmit Chagas disease [ 31 , 32 ].…”

Section: Introductionmentioning

confidence: 99%

Obligate development of Blastocrithidia papi (Trypanosomatidae) in the Malpighian tubules of Pyrrhocoris apterus (Hemiptera) and coordination of host-parasite life cycles

Frolov¹,

Malysheva²,

Ganyukova³

et al. 2018

PLoS ONE

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Blastocrithidia papi is a unique trypanosomatid in that its life cycle is synchronized with that of its host, and includes an obligate stage of development in Malpighian tubules (MTs). This occurs in firebugs, which exited the winter diapause. In the short period, preceding the mating of overwintered insects, the flagellates penetrate MTs of the host, multiply attached to the epithelial surface with their flagella, and start forming cyst-like amastigotes (CLAs) in large agglomerates. By the moment of oviposition, a large number of CLAs are already available in the rectum. They are discharged on the eggs' surface with feces, used for transmission of bugs' symbiotic bacteria, which are compulsorily engulfed by the newly hatched nymphs along with the CLAs. The obligate development of B. papi in MTs is definitely linked to the life cycle synchronization. The absence of peristalsis allow the trypanosomatids to accumulate and form dense CLA-forming subpopulations, whereas the lack of peritrophic structures facilitates the extensive discharge of CLAs directly into the hindgut lumen. The massive release of CLAs associated with oviposition is indispensable for maximization of the infection efficiency at the most favorable time point.

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“…The sequences of these two TUs differed from that of B. raabei by 4 substitutions and 1 indel (PNG12) and 8 substitutions and 1 indel (PNG78). Although there is no universally accepted similarity threshold for this molecular marker in trypanosomatids, this variation is certainly interspecific, since the two undoubtedly separate species (Blastocrithidia papi and B. largi) differ by only two substitutions in the whole sequences of this gene [29]. Meanwhile, the 18S rRNA gene sequences of B. raabei demonstrated variation in one nucleotide position, where C, T or a missing base were detected.…”

Section: Molecular Phylogenetic Analysesmentioning

confidence: 99%

“…are largely unknown [26]. There are only two exceptions: B. triatomae from the predatory triatomine bugs and B. papi from the omnivorous firebug Pyrrhocoris apterus [27][28][29][30].…”

Section: Introductionmentioning

confidence: 99%

If host is refractory, insistent parasite goes berserk: Trypanosomatid Blastocrithidia raabei in the dock bug Coreus marginatus

et al. 2020

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Here we characterized the development of the trypanosomatid Blastocrithidia raabei in the dock bug Coreus marginatus using light and electron microscopy. This parasite has been previously reported to occur in the host hemolymph, which is rather typical for dixenous trypanosomatids transmitted to a plant or vertebrate with insect's saliva. In addition, C. marginatus has an unusual organization of the intestine, which makes it refractory to microbial infections: two impassable segments isolate the anterior midgut portion responsible for digestion and absorption from the posterior one containing symbiotic bacteria. Our results refuted the possibility of hemolymph infection, but revealed that the refractory nature of the host provokes very aggressive behavior of the parasite and makes its life cycle more complex, reminiscent of that in some dixenous trypanosomatids. In the pre-barrier midgut portion, the epimastigotes of B. raabei attach to the epithelium and multiply similarly to regular insect trypanosomatids. However, when facing the impassable constricted region, the parasites rampage and either fiercely break through the isolating segments or attack the intestinal epithelium in front of the barrier. The cells of the latter group pass to the basal lamina and accumulate there, causing degradation of the epitheliocytes and thus helping the epimastigotes of the former group to advance posteriorly. In the symbiont-containing post-barrier midgut segment, the parasites either attach to bacterial cells and produce cyst-like amastigotes (CLAs) or infect enterocytes. In the rectum, all epimastigotes attach either to the cuticular lining or to each other and form CLAs. We argue that in addition to the specialized life cycle B. raabei possesses functional cell enhancements important either for the successful passage through the intestinal barriers (enlarged rostrum and well-developed Golgi complex) or as food reserves (vacuoles in the posterior end).

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Life cycle of Blastocrithidia papi sp. n. (Kinetoplastea, Trypanosomatidae) in Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae)

Cited by 22 publications

References 64 publications

The cotton stainer's gut microbiota suppresses infection of a cotransmitted trypanosomatid parasite

The cotton stainer's gut microbiota suppresses infection of a cotransmitted trypanosomatid parasite

Obligate development of Blastocrithidia papi (Trypanosomatidae) in the Malpighian tubules of Pyrrhocoris apterus (Hemiptera) and coordination of host-parasite life cycles

If host is refractory, insistent parasite goes berserk: Trypanosomatid Blastocrithidia raabei in the dock bug Coreus marginatus

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