Genetic Diversity and Phylogenetic Relationships of Coevolving Symbiont-Harboring Insect Trypanosomatids, and Their Neotropical Dispersal by Invader African Blowflies (Calliphoridae)

Abstract

This study is about the inter- and intra-specific genetic diversity of trypanosomatids of the genus Angomonas, and their association with Calliphoridae (blowflies) in Neotropical and Afrotropical regions. Microscopic examination of 3,900 flies of various families, mostly Calliphoridae, revealed that 31% of them harbored trypanosomatids. Small subunit rRNA (SSU rRNA) barcoding showed that Angomonas predominated (46%) over the other common trypanosomatids of blowflies of genera Herpetomonas and Wallacemonas. Among Angomonas spp., A. deanei was much more common than the two-other species, A. desouzai and A. ambiguus. Phylogenetic analyses based on SSU rRNA, glycosomal glyceraldehyde-3-phosphate dehydrogenase (gGAPDH) and internal transcribed spacer rDNA (ITS rDNA) sequences revealed a marked genetic diversity within A. deanei, which comprised four infraspecific genotypes (Dea1–Dea4), and four corresponding symbiont genotypes (Kcr1–Kcr4). Host and symbiont phylogenies were highly congruent corroborating their co-divergence, consistent with host-symbiont interdependent metabolism and symbiont reduced genomes shaped by a long coevolutionary history. We compared the diversity of Angomonas/symbionts from three genera of blowflies, Lucilia, Chrysomya and Cochliomyia. A. deanei, A. desouzai, and A. ambiguus were found in the three genera of blowflies in South America. In Africa, A. deanei and A. ambiguus were identified in Chrysomya. The absence of A. desouzai in Africa and its presence in Neotropical Cochliomyia and Lucilia suggests parasite spillback of A. desouzai into Chrysomya, which was most likely introduced four decades ago from Africa into the Neotropic. The absence of correlation between parasite diversity and geographic and genetic distances, with identical genotypes of A. deanei found in the Neotropic and Afrotropic, is consistent with disjunct distribution due to the recent human-mediated transoceanic dispersal of Angomonas by Chrysomya. This study provides the most comprehensive data gathered so far on the genetic repertoires of a genus of trypanosomatids found in flies from a wide geographical range.

High Prevalence and Endemism of Trypanosomatids on a Small Caribbean Island

“…However, our finding that in the heteropterans of Curac ßao 7 out of 9 (78%) trypanosomatid TUs were not previously described was unexpected, even if we take into account a possible bias caused by limited sampling and the disputable inclusion of two new TUs of the genus Blastocrithidia. This finding is even more surprising given that the diversity of South American trypanosomatids has been extensively studied (Borghesan et al 2013(Borghesan et al , 2018Jirk u et al 2012;Kozminsky et al 2015;Maslov et al 2007Maslov et al , 2010Teixeira et al 2011;Westenberger et al 2004;Yurchenko et al 2006), especially as compared to their Asian, African and Australian counterparts (Barratt et al 2017;Vot ypka et al 2010). Consequently, we expected the probability of finding a new TU in the Neotropics to be rather low.…”

“…Heteropteran insects of 11 different families belonging to 16 genera and 17 species were examined for the presence of trypanosomatid parasites. Out of 246 dissected true bugs, 93 (37.8%) individuals were infected by trypanosomatids (Tables 1 and 2), a prevalence much higher than the average global one, which for these obligatory parasites or less frequently commensals varies between 5 and 25% for true bugs (Heteroptera) (Borghesan et al 2018;Luke s et al 2018).…”

“…Out of 246 dissected true bugs, 93 (37.8%) individuals were infected by trypanosomatids (Tables and ), a prevalence much higher than the average global one, which for these obligatory parasites or less frequently commensals varies between 5 and 25% for true bugs (Heteroptera) (Borghesan et al. ; Lukeš et al. ).…”

“…Due to the scarcity of data on trypanosomatid infections in dipteran flies (Borghesan et al. , ; Hamilton et al. ; Teixeira et al.…”

The novel Dbl homology/BAR domain protein, MsgA, of Talaromyces marneffei regulates yeast morphogenesis during growth inside host cells

“…These play crucial roles in processes associated with cell shape such as control of polarized growth and cytoskeletal organisation. Rho-type GEFs are responsible for activating their small GTPase targets and their activity has been shown to regulate cytokinesis, cell wall integrity, antifungal resistance, viability, tissue invasive growth, mycotoxin production and virulence 11 – 14 . The majority of these studies have focused on GEFs containing canonical structural domains—a catalytic D bl h omology domain (DH) domain and an auxiliary p lekstrin h omology (PH) domain, excluding the contribution of GEFs with alternate domain structures (reviewed in 15 ).…”