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Species association of hepatitis B virus (HBV) in non-human apes; evidence for recombination between gorilla and chimpanzee variants.

Lyons S, Sharp C, LeBreton M, Djoko CF, Kiyang JA, Lankester F, Bibila TG, Tamoufé U, Fair J, Wolfe ND, Simmonds P - PLoS ONE (2012)

Bottom Line: Hepatitis B virus (HBV) infections are widely distributed in humans, infecting approximately one third of the world's population.Complete genome sequences were obtained from six of the infected chimpanzee and both gorillas; those from P. t .ellioti grouped with previously characterised variants from this subspecies.Both of these observations provide evidence for circulation of HBV between different species and sub-species of non-human primates, a conclusion that differs from the hypothesis if of strict host specificity of HBV genotypes.

View Article: PubMed Central - PubMed

Affiliation: Centre for Immunology, Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom. S.M.K.Lyons@sms.ed.ac.uk

ABSTRACT
Hepatitis B virus (HBV) infections are widely distributed in humans, infecting approximately one third of the world's population. HBV variants have also been detected and genetically characterised from Old World apes; Gorilla gorilla (gorilla), Pan troglodytes (chimpanzee), Pongo pygmaeus (orang-utan), Nomascus nastusus and Hylobates pileatus (gibbons) and from the New World monkey, Lagothrix lagotricha (woolly monkey). To investigate species-specificity and potential for cross species transmission of HBV between sympatric species of apes (such as gorillas and chimpanzees in Central Africa) or between humans and chimpanzees or gorillas, variants of HBV infecting captive wild-born non-human primates were genetically characterised. 9 of 62 chimpanzees (11.3%) and two from 11 gorillas (18%) were HBV-infected (15% combined frequency), while other Old world monkey species were negative. Complete genome sequences were obtained from six of the infected chimpanzee and both gorillas; those from P. t .ellioti grouped with previously characterised variants from this subspecies. However, variants recovered from P. t. troglodytes HBV variants also grouped within this clade, indicative of transmission between sub-species, forming a paraphyletic clade. The two gorilla viruses were phylogenetically distinct from chimpanzee and human variants although one showed evidence for a recombination event with a P.t.e.-derived HBV variant in the partial X and core gene region. Both of these observations provide evidence for circulation of HBV between different species and sub-species of non-human primates, a conclusion that differs from the hypothesis if of strict host specificity of HBV genotypes.

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Phylogenetic analysis based on the HBV genome and identified recombinant region 1560–2120 bp.Phylograms displaying phylogenetic trees based on (a) complete HBV genome; (c) HBV recombinant region 1560–2120 bp and equivalent fragments immediately preceding; (b) 999–1559 bp and succeeding; (d) 2121–2681 bp this region; with HBV reference sequences from human genotypes (A–H). Relative species and sub-species HBV variants are identified as follows Pan troglodytes troglodytes▴, Pan troglodytes ellioti▾, Pan troglodytes verus▪, Pan troglodytes schweinfurthii♦, Gorilla gorilla○ and Hylobates spp. □, and the host specific cluster is identified by ]. The trees were rooted with the woolly monkey HBV sequence, NC_001896▿. Sequences from this study are in bold and underlined and while recombinant HBV variants have bold branches.
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pone-0033430-g001: Phylogenetic analysis based on the HBV genome and identified recombinant region 1560–2120 bp.Phylograms displaying phylogenetic trees based on (a) complete HBV genome; (c) HBV recombinant region 1560–2120 bp and equivalent fragments immediately preceding; (b) 999–1559 bp and succeeding; (d) 2121–2681 bp this region; with HBV reference sequences from human genotypes (A–H). Relative species and sub-species HBV variants are identified as follows Pan troglodytes troglodytes▴, Pan troglodytes ellioti▾, Pan troglodytes verus▪, Pan troglodytes schweinfurthii♦, Gorilla gorilla○ and Hylobates spp. □, and the host specific cluster is identified by ]. The trees were rooted with the woolly monkey HBV sequence, NC_001896▿. Sequences from this study are in bold and underlined and while recombinant HBV variants have bold branches.

Mentions: Phylogenetic analysis of the HBV strains using 415 bp S gene fragments confirmed the grouping of the novel chimpanzee HBV strains with previously published HBV chimpanzee sequences and the grouping of the two novel gorilla HBV sequences with previously published HBV strains AJ131657 and FJ98095-97 [19], [21]. (The novel HBV sequence ECO50065LIP3J and FJ98095 were retrospectively identified as originating from the same gorilla in Limbe Wildlife Centre) (Data not shown). Mitochondrial sequencing confirmed that the ECO50083LIP5, ECO50210LIP4, ECO51394CWP1.4, ECO51377CWP2 and ECO51109CWP4, ECO51212CWP6 HBV variants originated from chimpanzee subspecies P. t. ellioti and P. t. troglodytes respectively, while ECO50003LIP3 and ECO50065LIP3 were identified as gorilla-derived (Table 1). Complete genome sequencing of the eight study isolates produced sequences of 3182-bp in length, comparable to reference chimpanzee and gorilla strains (Fig 1). Phylogenetic analysis based on the complete genome (Fig. 1a), demonstrated monophyletic groupings for each human genotype (A–H), a clade containing gibbon and orangutans variants and a third containing chimpanzee and gorilla HBV sequences, each supported by high bootstrap values. Sequences of all novel chimpanzee HBV variants, irrespective of their sub species specific host, clustered with HBV sequences previously obtained from P. t. ellioti[21]. As the study samples were obtained from captive settings where P. t. troglodytes and P. t. ellioti are frequently co-housed, it remains unclear whether these findings reflect the HBV genotype distribution among wild chimpanzees in Cameroon or whether infection of troglodytes by ellioti-derived strains occurred in captivity.


Species association of hepatitis B virus (HBV) in non-human apes; evidence for recombination between gorilla and chimpanzee variants.

Lyons S, Sharp C, LeBreton M, Djoko CF, Kiyang JA, Lankester F, Bibila TG, Tamoufé U, Fair J, Wolfe ND, Simmonds P - PLoS ONE (2012)

Phylogenetic analysis based on the HBV genome and identified recombinant region 1560–2120 bp.Phylograms displaying phylogenetic trees based on (a) complete HBV genome; (c) HBV recombinant region 1560–2120 bp and equivalent fragments immediately preceding; (b) 999–1559 bp and succeeding; (d) 2121–2681 bp this region; with HBV reference sequences from human genotypes (A–H). Relative species and sub-species HBV variants are identified as follows Pan troglodytes troglodytes▴, Pan troglodytes ellioti▾, Pan troglodytes verus▪, Pan troglodytes schweinfurthii♦, Gorilla gorilla○ and Hylobates spp. □, and the host specific cluster is identified by ]. The trees were rooted with the woolly monkey HBV sequence, NC_001896▿. Sequences from this study are in bold and underlined and while recombinant HBV variants have bold branches.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3303819&req=5

pone-0033430-g001: Phylogenetic analysis based on the HBV genome and identified recombinant region 1560–2120 bp.Phylograms displaying phylogenetic trees based on (a) complete HBV genome; (c) HBV recombinant region 1560–2120 bp and equivalent fragments immediately preceding; (b) 999–1559 bp and succeeding; (d) 2121–2681 bp this region; with HBV reference sequences from human genotypes (A–H). Relative species and sub-species HBV variants are identified as follows Pan troglodytes troglodytes▴, Pan troglodytes ellioti▾, Pan troglodytes verus▪, Pan troglodytes schweinfurthii♦, Gorilla gorilla○ and Hylobates spp. □, and the host specific cluster is identified by ]. The trees were rooted with the woolly monkey HBV sequence, NC_001896▿. Sequences from this study are in bold and underlined and while recombinant HBV variants have bold branches.
Mentions: Phylogenetic analysis of the HBV strains using 415 bp S gene fragments confirmed the grouping of the novel chimpanzee HBV strains with previously published HBV chimpanzee sequences and the grouping of the two novel gorilla HBV sequences with previously published HBV strains AJ131657 and FJ98095-97 [19], [21]. (The novel HBV sequence ECO50065LIP3J and FJ98095 were retrospectively identified as originating from the same gorilla in Limbe Wildlife Centre) (Data not shown). Mitochondrial sequencing confirmed that the ECO50083LIP5, ECO50210LIP4, ECO51394CWP1.4, ECO51377CWP2 and ECO51109CWP4, ECO51212CWP6 HBV variants originated from chimpanzee subspecies P. t. ellioti and P. t. troglodytes respectively, while ECO50003LIP3 and ECO50065LIP3 were identified as gorilla-derived (Table 1). Complete genome sequencing of the eight study isolates produced sequences of 3182-bp in length, comparable to reference chimpanzee and gorilla strains (Fig 1). Phylogenetic analysis based on the complete genome (Fig. 1a), demonstrated monophyletic groupings for each human genotype (A–H), a clade containing gibbon and orangutans variants and a third containing chimpanzee and gorilla HBV sequences, each supported by high bootstrap values. Sequences of all novel chimpanzee HBV variants, irrespective of their sub species specific host, clustered with HBV sequences previously obtained from P. t. ellioti[21]. As the study samples were obtained from captive settings where P. t. troglodytes and P. t. ellioti are frequently co-housed, it remains unclear whether these findings reflect the HBV genotype distribution among wild chimpanzees in Cameroon or whether infection of troglodytes by ellioti-derived strains occurred in captivity.

Bottom Line: Hepatitis B virus (HBV) infections are widely distributed in humans, infecting approximately one third of the world's population.Complete genome sequences were obtained from six of the infected chimpanzee and both gorillas; those from P. t .ellioti grouped with previously characterised variants from this subspecies.Both of these observations provide evidence for circulation of HBV between different species and sub-species of non-human primates, a conclusion that differs from the hypothesis if of strict host specificity of HBV genotypes.

View Article: PubMed Central - PubMed

Affiliation: Centre for Immunology, Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom. S.M.K.Lyons@sms.ed.ac.uk

ABSTRACT
Hepatitis B virus (HBV) infections are widely distributed in humans, infecting approximately one third of the world's population. HBV variants have also been detected and genetically characterised from Old World apes; Gorilla gorilla (gorilla), Pan troglodytes (chimpanzee), Pongo pygmaeus (orang-utan), Nomascus nastusus and Hylobates pileatus (gibbons) and from the New World monkey, Lagothrix lagotricha (woolly monkey). To investigate species-specificity and potential for cross species transmission of HBV between sympatric species of apes (such as gorillas and chimpanzees in Central Africa) or between humans and chimpanzees or gorillas, variants of HBV infecting captive wild-born non-human primates were genetically characterised. 9 of 62 chimpanzees (11.3%) and two from 11 gorillas (18%) were HBV-infected (15% combined frequency), while other Old world monkey species were negative. Complete genome sequences were obtained from six of the infected chimpanzee and both gorillas; those from P. t .ellioti grouped with previously characterised variants from this subspecies. However, variants recovered from P. t. troglodytes HBV variants also grouped within this clade, indicative of transmission between sub-species, forming a paraphyletic clade. The two gorilla viruses were phylogenetically distinct from chimpanzee and human variants although one showed evidence for a recombination event with a P.t.e.-derived HBV variant in the partial X and core gene region. Both of these observations provide evidence for circulation of HBV between different species and sub-species of non-human primates, a conclusion that differs from the hypothesis if of strict host specificity of HBV genotypes.

Show MeSH
Related in: MedlinePlus