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First Molecular Detection of Polychromophilus Parasites in Brazilian Bat Species.

ABSTRACT: Blood parasites of the Haemosporida order, such as the Plasmodium spp. responsible for malaria, have become the focus of many studies in evolutionary biology. However, there is a lack of molecular investigation of haemosporidian parasites of wildlife, such as the genus Polychromophilus. Species of this neglected genus exclusively have been described in bats, mainly in Europe, Asia, and Africa, but little is known about its presence and genetic diversity on the American continent. Here, we investigated 406 bats from sites inserted in remnant fragments of the Atlantic Forest and Cerrado biomes and urbanized areas from southern Brazil for the presence of Polychromophilus species by PCR of the mitochondrial cytochrome b encoding gene. A total of 1.2% of bats was positive for Polychromophilus, providing the first molecular information of these parasites in Myotis riparius and Eptesicus diminutus, common vespertilionid bats widely distributed in different Brazilian biomes, and Myotis ruber, an endangered species. A Bayesian analysis was conducted to reconstruct the phylogenetic relationships between Polychromophilus recovered from Brazilian bats and those identified elsewhere. Sequences of Brazilian Polychromophilus lineages were placed with P. murinus and in a clade distinct from P. melanipherus, mainly restricted to bats in the family Vespertilionidae. However, the sequences were split into two minor clades, according to the genus of hosts, indicating that P. murinus and a distinct species may be circulating in Brazil. Morphological observations combined with additional molecular studies are needed to conclude and describe these Polychromophilus species.

SUBMITTER: Minozzo GA

PROVIDER: S-EPMC8230147 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Malaria parasites in the phylum Apicomplexa (Order: Haemosporida) infect diverse vertebrates and invertebrate hosts. At least seven genera of haemosporidian parasites have been described to exclusively infect bats. Most of these parasites remain enigmatic with a poorly known host range. Here, we investigated 271 bats belonging to 21 species and seven families from six provinces of Thailand. Overall, 124 out of 271 bats (45.8%) were positive for haemosporidian parasites, while none had Plasmodium, based on microscopic examination of blood smears and PCR amplification. We obtained 19 distinct cytochrome b (cytb) nucleotide haplotypes of Hepatocystis from seven bat species (families: Craseonycteridae, Hipposideridae, Pteropodidae, and Rhinolophidae). Nycteria was found in four bat species (Craseonycteridae, Emballonuridae, Megadermatidae, and Pteropodidae) and Polychromophilus in two species (Emballonuridae, Vespertilionidae). Phylogenetic analysis inferred from cytb sequences placed Hepatocystis into 2 different clades. Most Hepatocystis infections were found in insectivorous bats and clustered together with a sequence from Hipposideros larvatus in Cambodia (in subclade 1a). A single sequence of Hepatocystis obtained from a frugivorous bat, Cynopterus brachyotis, was placed in the same clade with Hepatocystis from the same bat species previously reported in Malaysia (clade 2). Nycteria in these Thai bats were clearly separated from the African isolates previously reported in bats in the family Rhinolophidae. Polychromophilus murinus from Myotis siligorensis was placed in a distinct clade (clade 2) from Polychromophilus melanipherus isolated from Taphozous melanopogon (clade 1). These results confirmed that at least two distinct species of Polychromophilus are found in Thailand. Collectively, Hepatocystis presented no host specificity. Although Megaderma spasma seemed to be infected by only Nycteria, its respective parasite does not show specificity to only a single bat host. Polychromophilus murinus and P. melanipherus seem to infect a narrower host range or are somehow restricted to bats in the families Vespertilionidae and Emballonuridae, respectively.

Project description:BackgroundHaemosporidian parasites of the genus Polychromophilus infect bats worldwide. They are vectored by obligate ectoparasitic bat flies of the family Nycteribiidae. Despite their global distribution, only five Polychromophilus morphospecies have been described to date. The two predominant species, Polychromophilus melanipherus and Polychromophilus murinus, are broadly distributed and mainly infect miniopterid and vespertilionid bats, respectively. In areas where species from different bat families aggregate together, the infection dynamics and ability of either Polychromophilus species to infect other host families is poorly characterized.MethodsWe collected 215 bat flies from two bat species, Miniopterus schreibersii and Rhinolophus ferrumequinum, which sometimes form mixed clusters in Serbia. Miniopterus schreibersii is known to be frequently infected with P. melanipherus, whereas R. ferrumequinum has been observed to be incidentally infected with both Polychromophilus species. All flies were screened for Polychromophilus infections using a PCR targeting the haemosporidian cytb gene. Positive samples were subsequently sequenced for 579 bp of cytochrome b (cytb) and 945 bp of cytochrome oxidase subunit 1 (cox1).ResultsPolychromophilus melanipherus DNA was detected at six out of nine sampling locations and in all three examined bat fly species collected from M. schreibersii (Nycteribia schmidlii, n = 21; Penicillidia conspicua, n = 8; Penicillidia dufourii, n = 3). Four and five haplotypes were found for cytb and cox1, respectively. Evidence for multiple Polychromophilus haplotypes was found in 15 individual flies. These results point to a high diversity of P. melanipherus parasites in Miniopterus hosts and efficient transmission throughout the study area. A single Phthiridium biarticulatum bat fly collected from R. ferrumequinum screened positive for P. melanipherus, but only yielded a partial cox1 sequence fragment. Nevertheless, this result suggests that secondary hosts (both bat and fly species) are regularly confronted with this parasite.ConclusionsThe results of this study provide new insights into the prevalence and distribution of Polychromophilus parasites in European bats and their nycteribiid vectors. The use of bat flies for the non-invasive investigation of Polychromophilus infections in bat populations has proven to be efficient and thus represents an alternative for large-scale studies of infections in bat populations without the need to invasively collect blood from bats.

Project description:In recent phylogenetic studies, bat Polychromophilus and ungulate Plasmodium, two relatively understudied haemosporidian parasites within the Apicomplexa phylum, have often been overlooked. Instead, the focus has been primarily on haemosporidian parasites in primates, rodents, and birds. Several phylogenetic analyses of bat Polychromophilus have relied on limited datasets and short informative DNA sequences. As a result of these inherent limitations, the substantiation of their evolutionary stance has encountered a diminished degree of robust validation. This study successfully obtained complete mitochondrial genome sequences from 11 Polychromophilus parasites originating from Hipposideros gentilis and Myotis siligoensis bats for the first time. Additionally, the authors have sequenced the apicoplast caseinolytic protease C genes from Polychromophilus murinus and a potentially new Polychromophilus species. These mitochondrial genomes range in length from 5994 to 6001 bp and consist of three protein-coding genes (PCGs), seven small subunit ribosomal RNA genes (SSU rRNA), 12 large subunit ribosomal RNA genes (LSU rRNA), and seven miscellaneous RNA genes. Phylogenetic analyses using Bayesian Inference and Maximum Likelihood methods indicated robust support for the grouping of ungulate Plasmodium and bat Polychromophilus in a single clade separate from other Plasmodium spp., confirming previous reports, albeit with stronger evidence in this study. The divergence between Polychromophilus in bats and Plasmodium in ungulates occurred approximately 29.61 to 55.77 million years ago (Mya), with a node age estimated at 40.63 Mya. These findings highlight that the genus Plasmodium, which includes species found in ungulates, birds, reptiles, and other mammals, does not form a monophyletic group. By incorporating Polychromophilus in bats and Plasmodium in ungulates, this study contributes significantly to understanding the phylogenetic relationships within the Haemosporida order. It provides valuable insights into the evolutionary history and interconnections among these diverse parasites, thereby expanding knowledge in this field.

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First Molecular Detection of Polychromophilus Parasites in Brazilian Bat Species.

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