High prevalence of trypanosome co-infections in freshwater fishes

Grybchuk-Ieremenko, Anastasiia; Losev, Alexander; Kostygov, Alexei Y.; Lukeš, Julius; Yurchenko, Vyacheslav

doi:10.14411/fp.2014.064

Cited by 39 publications

(44 citation statements)

References 55 publications

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“…Our description of parasite cooccurrence patterns provides critical new insights into disease ecology, as parasite associations are expected across many host systems (Bell et al 2006;P erez-Tris et al 2007;Johnson & Buller 2011;Vaumourin et al 2015), yet evidence from wildlife is biased towards mammalian hosts (Lello et al 2004;Tompkins et al 2011;Hellard et al 2015). Additionally, we show that co-infections are difficult to identify using PCR alone, a finding demonstrated for many host-pathogen systems (Valki unas et al 2006;Dyachenko et al 2010;Grybchuk-Ieremenko et al 2014;Moustafa et al 2016). We overcame this hurdle by combining traditional and molecular parasitology methods, a multidisciplinary approach that we recommend for future work on wildlife co-infections.…”

Section: Discussionmentioning

confidence: 69%

Co‐infections and environmental conditions drive the distributions of blood parasites in wild birds

Clark

Wells

Dimitrov

et al. 2016

Journal of Animal Ecology

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Summary 1.Experimental work increasingly suggests that non-random pathogen associations can affect the spread or severity of disease. Yet due to difficulties distinguishing and interpreting co-infections, evidence for the presence and directionality of pathogen co-occurrences in wildlife is rudimentary. 2. We provide empirical evidence for pathogen co-occurrences by analysing infection matrices for avian malaria (Haemoproteus and Plasmodium spp.) and parasitic filarial nematodes (microfilariae) in wild birds (New Caledonian Zosterops spp.). 3. Using visual and genus-specific molecular parasite screening, we identified high levels of co-infections that would have been missed using PCR alone. Avian malaria lineages were assigned to species level using morphological descriptions. We estimated parasite co-occurrence probabilities, while accounting for environmental predictors, in a hierarchical multivariate logistic regression. 4. Co-infections occurred in 36% of infected birds. We identified both positively and negatively correlated parasite co-occurrence probabilities when accounting for host, habitat and island effects. Two of three pairwise avian malaria co-occurrences were strongly negative, despite each malaria parasite occurring across all islands and habitats. Birds with microfilariae had elevated heterophil to lymphocyte ratios and were all co-infected with avian malaria, consistent with evidence that host immune modulation by parasitic nematodes facilitates malaria co-infections. Importantly, co-occurrence patterns with microfilariae varied in direction among avian malaria species; two malaria parasites correlated positively but a third correlated negatively with microfilariae. 5. We show that wildlife co-infections are frequent, possibly affecting infection rates through competition or facilitation. We argue that combining multiple diagnostic screening methods with multivariate logistic regression offers a platform to disentangle impacts of environmental factors and parasite co-occurrences on wildlife disease.

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Section: Discussionmentioning

confidence: 69%

Co‐infections and environmental conditions drive the distributions of blood parasites in wild birds

Clark

Wells

Dimitrov

et al. 2016

Journal of Animal Ecology

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“…), whereas divergent DNA sequences corresponding to more than one species (mixed infections) can be obtained from fish blood samples exhibiting similar trypomastigote morphotypes (Grybchuk‐Ieremenko et al. ; Lemos et al. ).…”

Section: Resultsmentioning

confidence: 99%

Developmental and Ultrastructural Characterization and Phylogenetic Analysis of Trypanosoma herthameyeri n. sp. of Brazilian Leptodactilydae Frogs

Attias

Sato

Ferreira

et al. 2016

J Eukaryotic Microbiology

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We described the phylogenetic affiliation, development in cultures and ultrastructural features of a trypanosome of Leptodacylus chaquensis from the Pantanal biome of Brazil. In the inferred phylogeny, this trypanosome nested into the Anura clade of the basal Aquatic clade of Trypanosoma, but was separate from all known species within this clade. This finding enabled us to describe it as Trypanosoma herthameyeri n. sp., which also infects other Leptodacylus species from the Pantanal and Caatinga biomes. Trypanosoma herthameyeri multiplies as small rounded forms clumped together and evolving into multiple-fission forms and rosettes of epimastigotes released as long forms with long flagella; scarce trypomastigotes and glove-like forms are common in stationary-phase cultures. For the first time, a trypanosome from an amphibian was observed by field emission scanning electron microscopy, revealing a cytostome opening, well-developed flagellar lamella, and many grooves in pumpkin-like forms. Transmission electron microscopy showed highly developed Golgi complexes, relaxed catenation of KDNA, and a rich set of spongiome tubules in a regular parallel arrangement to the flagellar pocket as confirmed by electron tomography. Considering the basal position in the phylogenetic tree, developmental and ultrastructural data of T. herthameyeri are valuable for evolutionary studies of trypanosome architecture and cell biology.

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“…Since mixed trypanosome infections are common in wild‐caught fish (Grybchuk‐Ieremenko et al. ; Lemos et al. ), it is always necessary to ensure the use of single parasite isolates in biological studies (Fermino et al.…”

Section: Discussionmentioning

confidence: 99%

“…; Grybchuk‐Ieremenko et al. ; Lemos et al. ), which is now possible, due to the advances in distinct technologies based on molecular techniques (Fermino et al.…”

Section: Discussionmentioning

confidence: 99%

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In Vitro Cellular Division of Trypanosoma abeli Reveals Two Pathways for Organelle Replication

Borges

Toledo

Fermino³

et al. 2018

J Eukaryotic Microbiology

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Since the observation of the great pleomorphism of fish trypanosomes, in vitro culture has become an important tool to support taxonomic studies investigating the biology of cultured parasites, such as their structure, growth dynamics, and cellular cycle. Relative to their biology, ex vivo and in vitro studies have shown that these parasites, during the multiplication process, duplicate and segregate the kinetoplast before nucleus replication and division. However, the inverse sequence (the nucleus divides before the kinetoplast) has only been documented for a species of marine fish trypanosomes on a single occasion. Now, this previously rare event was observed in Trypanosoma abeli, a freshwater fish trypanosome. Specifically, from 376 cultured parasites in the multiplication process, we determined the sequence of organelle division for 111 forms; 39% exhibited nucleus duplication prior to kinetoplast replication. Thus, our results suggest that nucleus division before the kinetoplast may not represent an accidental or erroneous event occurring in the main pathway of parasite reproduction, but instead could be a species-specific process of cell biology in trypanosomes, such as previously noticed for Leishmania. This "alternative" pathway for organelle replication is a new field to be explored concerning the biology of marine and freshwater fish trypanosomes.

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High prevalence of trypanosome co-infections in freshwater fishes

Cited by 39 publications

References 55 publications

Co‐infections and environmental conditions drive the distributions of blood parasites in wild birds

Co‐infections and environmental conditions drive the distributions of blood parasites in wild birds

Developmental and Ultrastructural Characterization and Phylogenetic Analysis of Trypanosoma herthameyeri n. sp. of Brazilian Leptodactilydae Frogs

In Vitro Cellular Division of Trypanosoma abeli Reveals Two Pathways for Organelle Replication

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