ReviewBabesia: A world emerging
Graphical abstract
Highlights
► Relevant Babesia parasites of man, and domestic and wildlife animals are introduced. ► Evolution scenarios of piroplasmids in relation to vertebrates and ticks are offered. ► An improved phylogenetic classification of major piroplasmid lineages is presented. ► The classical and molecular taxonomy of Babesia species is reviewed. ► The significance of recent population genetic findings is summarized.
Introduction
Babesia are tick-transmitted protozoan hemoparasites, of great economic, veterinary and medical impact worldwide. They are considered to be the second most commonly found parasites in the blood of mammals after trypanosomes, and they have also been described infecting birds. In their vertebrate hosts they reproduce asexually inside erythrocytes, and together with Theileria spp. they are referred to as piroplasms or piroplasmids. The sexual phase of the Babesia life cycle typically takes place in Ixodid ticks, which acquire and transmit the parasites during their blood meals (Fig. 1) (Kakoma and Mehlhorn, 1994, Telford et al., 1993, Gray and Weiss, 2008).
Victor Babeş (1888) was the first to discover microorganisms inside bovine erythrocytes of Romanian cattle that presented hemoglobinuria; and he later observed a similar organism in sheep blood (Babeş, 1892). Five years later in the USA, Smith and Kilbour described that the presence of an intraerythrocytic parasite was the cause of tick-transmitted Texas Cattle Fever, a disease that had long stricken cattle ranchers in the Southern US states (Smith and Kilbourne, 1893). This turned out to be the first description of an arthropod-transmitted pathogen of vertebrates. The parasites described by Babeş, and Smith and Kilbour were later named Babesia bovis, B. ovis and B. bigemina, respectively (Starcovici, 1893, Mihalca, 2010). Soon afterwards, babesias parasitizing the blood of other domestic animals were observed, such as those that eventually became known as B. canis and B. caballi, described by Piana and Galli-Valerio (1895) and by Koch (1904), in dog and horse erythrocytes, respectively. Since these early findings, more than 100 different Babesia species have been discovered, and thanks to the advances in microscopy, cell biology and molecular biology techniques our knowledge of the Babesia world is rapidly expanding (Levine, 1988, Roncalli Amici, 2001, Criado-Fornelio et al., 2004, De Waal and Van Heerden, 2004, Uilenberg, 2006, Lack et al., 2012).
Section snippets
Distribution and pathological effects of some relevant Babesia spp.
The remarkable impact of babesia infections in three host groups: domestic animals, humans and, most recently acknowledged, some wildlife species, has inspired a great amount of research efforts in recent decades.
In general, babesia infections course with varying degrees of severity that can often be associated to the host’s age, immunological status, concurrent infections with other pathogens, and/or genetic factors. Common manifestations of acute babesia infections in different hosts can
The natural history of Babesia
To gain some insight into the nature of co-evolution and interaction between apicomplexan piroplasmids and their invertebrate and vertebrate hosts, an inevitably tentative view of their evolutionary history is outlined here based on recent research findings. Comparative morphology suggests that the most recent common ancestor (MRCA) of apicomplexans (which include gregarines, piroplasmids, Plasmodium, coccidians, cryptosporidia, etc.) possessed a prevailing presence in marine environments, with
Classical taxonomy
The group comprising Babesia and Theileria has been baptized “piroplasmids” due to the pear-shaped morphology of the multiplying parasite stage in the blood of the vertebrate host. As non-pigment forming hemoparasites, piroplasmids can be further distinguished from other erythrocyte-infecting genera, such as Plasmodium and Haemoproteus, which in contrast form pigment (hemozoin) in the parasitized cell (Uilenberg, 2006).
Before the application of molecular methodologies, no less than 111 valid
Tracing the ancestors: the 18S rRNA gene
In contrast to phenotypic characters, those derived from molecular sequences have the advantage of differentiating morphologically similar species and quantifying these differences. Recently, molecular phylogeny has made and will continue to make major contributions towards revealing evolutionary lineages and relations, and suggesting classification of piroplasmids. Importantly, these contributions have largely confirmed previous taxonomic classifications, based on a limited number of
Molecular taxonomy
As has been outlined above, the identification and definition of an increasing number of piroplasmid lineages and species cannot be achieved by the relatively few available phenotypic characters. As a steadily increasing number of piroplasmid species are described, molecular taxonomic approaches to define and outline species and higher taxon boundaries will become increasingly important (Blaxter, 2004; Blaxter et al., 2005, DeSalle et al., 2005, Hajibabaei et al., 2007). It is essential to
Population genetics
Population genetics provides important insights into the genetic diversity, population dynamics, and structure of parasite populations. As these parameters describe the adaptation of the parasite population for survival in response to environmental challenges, they have a major impact on vaccination strategies, as well as on the understanding of drug resistance, epidemiology, and pathogenicity (Beck et al., 2009a). The advent of molecular genetics and genomics, specifically PCR-based
Concluding remarks
We have presented a comprehensive summary of recent research findings that outline and integrate the important historic events of piroplasmid evolution in relation to their tick and vertebrate hosts. A novel improved classification of major piroplasmid lineages has been proposed based on an extensive molecular phylogenetic analysis of the 18S rRNA gene. The classic taxonomy of Babesia parasites, as well as Theileria and Cytauxzoon, was discussed, and recent developments of molecular taxonomy,
Acknowledgments
Financial support from the National Research Council of Argentina (CONICET), the National Institute of Technological Agriculture (INTA, AESA 203961 and AERG 232152), and the European Commission (INCO 245145, PIROVAC), as well as the assistance of Daniela Flores, are gratefully acknowledged.
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