Abstract
We report the first de novo sequence assembly and analysis of the genome of Testudinid herpesvirus 3 (TeHV3), one of the most pathogenic chelonian herpesviruses. The genome of TeHV3 is at least 150,080 nucleotides long, is arranged in a type D configuration and comprises at least 102 open reading frames extensively co-linear with those of Human herpesvirus 1. Consistently, the phylogenetic analysis positions TeHV3 among the Alphaherpesvirinae, closely associated with Chelonid herpesvirus 5, a Scutavirus. To date, there has been limited genetic characterization of TeHVs and a resolution beyond the genotype was not feasible because of the lack of informative DNA sequences. To exemplify the potential benefits of the novel genomic information provided by this first whole genome analysis, we selected the glycoprotein B (gB) gene, for detailed comparison among different TeHV3 isolates. The rationale for selecting gB is that it encodes for a well-conserved protein among herpesviruses but is coupled with a relevant antigenicity and is consequently prone to accumulate single nucleotide polymorphisms. These features were considered critical for an ideal phylogenetic marker to investigate the potential existence of distinct TeHV3 genogroups and their associated pathology. Fifteen captive tortoises presumptively diagnosed to be infected with TeHVs or carrying compatible lesions on the basis of either the presence of intranuclear inclusions (presumptively infected) and/or diphtheronecrotic stomatitis-glossitis or pneumonia (compatible lesions) were selected for the study. Viral isolation, TeHV identification, phylogenetic analysis and pathological characterization of the associated lesions, were performed. Our results revealed 1) the existence of at least two distinct TeHV3 genogroups apparently associated with different pathologies in tortoises and 2) the first evidence for a putative homologous recombination event having occurred in a chelonian herpesvirus. This novel information is not only fundamental for the genetic characterization of this virus but is also critical to lay the groundwork for an improved understanding of host-pathogen interactions in chelonians and contribute to tortoise conservation.
Highlights
Herpesviruses have been reported as significant pathogens of snakes [1, 2], lizards [3,4,5,6,7,8,9,10] and alligators [11, 12], more herpesviruses have been detected in chelonians than in any other reptilian taxa [13]
The TeHV3 genome is composed of a unique long (UL) and a unique short (US) region, with the US flanked by inverted repeats consistent with a type D arrangement similar to that of Human herpesvirus 3 (HHV3-Varicella zoster virus (VZV)) and the recently described genome of Chelonid herpesvirus 5 (ChHV5) [22]
The two genomes share the overall arrangement and show the most similarities within the UL region. This is consistent with the findings of Alba et al (2001) [55], with the most conserved gene blocks in the Herpesviridae spanning from the UL5 to the UL39 homologues
Summary
Herpesviruses have been reported as significant pathogens of snakes [1, 2], lizards [3,4,5,6,7,8,9,10] and alligators [11, 12], more herpesviruses have been detected in chelonians than in any other reptilian taxa [13]. In the last few years an increasing number of novel herpesviruses have been detected in fresh water turtles. These include a herpesvirus infecting the Australian Krefft’s river turtles (Emydura macquarii kreftii) associated with proliferative and ulcerative tegument lesions [26] and Pelomedusid herpesvirus 1 in a clinically healthy West African mud turtle (Pelusios castaneous) [27]. Emydid herpesvirus 1 is a novel chelonian herpesvirus detected in an eastern river cooter (Pseudemys concinna concinna) with viral inclusions in the hepatocytes [28] and in both diseased (with pneumonia, hepatitis and splenitis) and clinically healthy northern map turtles (Graptmeys geographica) along with asymptomatic painted turtles [29]. Terrapene herpesvirus 1 was detected in captive eastern box turtles (Terrapene carolina carolina) with stomatitis and glossitis [31], whereas Terrapene herpesvirus 2 was recently identified in an eastern box turtle coinfected with a spirorchid trematode and with papillomatous growths [32]
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