Open Access

A novel adenovirus of Western lowland gorillas (Gorilla gorilla gorilla)

  • Diana Wevers1,
  • Fabian H Leendertz2,
  • Nelly Scuda1,
  • Christophe Boesch3,
  • Martha M Robbins3,
  • Josephine Head3,
  • Carsten Ludwig4,
  • Joachim Kühn5 and
  • Bernhard Ehlers1Email author
Virology Journal20107:303

https://doi.org/10.1186/1743-422X-7-303

Received: 1 September 2010

Accepted: 5 November 2010

Published: 5 November 2010

Abstract

Adenoviruses (AdV) broadly infect vertebrate hosts including a variety of primates. We identified a novel AdV in the feces of captive gorillas by isolation in cell culture, electron microscopy and PCR. From the supernatants of infected cultures we amplified DNA polymerase (DPOL), preterminal protein (pTP) and hexon gene sequences with generic pan primate AdV PCR assays. The sequences in-between were amplified by long-distance PCRs of 2 - 10 kb length, resulting in a final sequence of 15.6 kb. Phylogenetic analysis placed the novel gorilla AdV into a cluster of primate AdVs belonging to the species Human adenovirus B (HAdV-B). Depending on the analyzed gene, its position within the cluster was variable. To further elucidate its origin, feces samples of wild gorillas were analyzed. AdV hexon sequences were detected which are indicative for three distinct and novel gorilla HAdV-B viruses, among them a virus nearly identical to the novel AdV isolated from captive gorillas. This shows that the discovered virus is a member of a group of HAdV-B viruses that naturally infect gorillas. The mixed phylogenetic clusters of gorilla, chimpanzee, bonobo and human AdVs within the HAdV-B species indicate that host switches may have been a component of the evolution of human and non-human primate HAdV-B viruses.

Findings

Adenoviruses are non-enveloped icosahedral double-stranded DNA viruses that infect fish, amphibians, reptiles, birds and mammals [1]. Human adenoviruses (HAdV) are categorized into seven species (HAdV-A to HAdV-G) [2]. Each species includes a distinct number of serotypes [3]. In addition, intra-species shuffling of penton base, fiber and hexon genes by recombination has been frequently observed [46]. Simian adenoviruses have been discovered in monkeys and great apes [711]. They are very similar to HAdV, and most of them can be grouped into corresponding HAdV species or the newly established species Simian adenovirus A (SAdV-A).

In 2008, a group of Western lowland gorillas (Gorilla gorilla gorilla) suffered from prolonged diarrhea and self-limiting respiratory disease in the Zoological gardens of Münster, Germany. To isolate viral agents potentially responsible for the symptoms, fecal samples were suspended in phosphate-buffered saline, sterile filtered and cultured on MRC-5 cells and A549 cells. After eight days of culture, a cytopathogenic effect was observed. The culture supernatant was examined by electron microscopy, and virus-like structures were detected their size and general structure being consistent with that of adenoviruses (Additional Figure 1).

DNA was then extracted from culture supernatant using the Qiagen tissue kit according to the manufacturer's instructions (Qiagen, Hilden, Germany), and a generic primate adenovirus PCR was performed. For this purpose, a nested set of degenerate and deoxyinosine-substituted (deg/dI) primers was designed, targeting a highly conserved region of the DNA polymerase (DPOL) gene of primate mastadenoviruses (Figure 1; Table 1). PCR was performed in a total volume of 25 μl with 0.2 μl AmpliTaq Gold (Applied Biosystems), 20 pmol of each primer, 200 μM dNTPs, 2 mM MgCl2, and 5% DMSO. A T-Gradient thermocycler from Biometra was used with the following cycling conditions: 95°C for 12 min, and 45 cycles of 95°C for 30 sec, 45°C (1st round and 2nd round) for 30 sec and 72°C for 2 min, followed by a 15 min final extension step at 72°C. PCR products were purified using the Invisorb DNA clean up kit according to the instructions of the manufacturer (Invitek, Berlin, Germany), and directly sequenced with the Big Dye terminator cycle sequencing kit (Applied Biosystems, Warrington, UK) on a 377 automated DNA sequencer (Applied Biosystems). In BLAST analysis of GenBank, the sequence was most closely related to chimpanzee AdVs and human AdVs of the species HAdV-B. There was less similarity to the six gorilla HAdV-B viruses (SAdV-27.2; SAdV-28.2; SAdV-41.1; SAdV-41.2; SAdV-46; SAdV-47; Table 2) recently described [12]. Since the novel gorilla AdV was the seventh HAdV-B of this host, it was named for the purpose of this paper Gorilla gorilla adenovirus B7 (GgorAdV-B7).
Figure 1

PCR amplification strategy. Above the ruler, the amplified part of the AdV genome is depicted. Below, a schematic visualisation of the positions of the degenerated consensus PCRs (red lines), the long-distance PCRs (black lines) and the resulting contiguous sequence (blue line) is given. In the box, the hexon gene is magnified, and the positions of the hexon loops and the Hex-loop2 PCR (red line) are illustrated.

Table 1

Primers for amplification of DPOL, pTP and hexon gene sequences

Primer-set abbreviation

Targeted gene

Name of primer

sequence 5'-3'

PCR length

Annealing temp.

Degenerate primers

DPOL-cons

DPOL

4431-s $

GTnTwyGAyAThTGyGGhATGTAyGC

  
  

4428-as

GAGGCTGTCCGTrTC(n/i)CCGTA#

956 bp

45°C

  

4428-s

CGGACGCCTCTGyTGGAC(n/i)AA

  
  

4429-as

GGCCAGCACrAA(n/i)GArGC

650 bp

45°C

Hex-5'-cons

Hexon

4515-s

GTGGATGG(n/i)GA(r/i)GG(n/i)TACA

  
  

4515-as

CGCACAACGTC(r/i)AA(n/i)AC(y/i)TC

536 bp

45°C

  

4516-s

TGTAACATGAC(y/i)AA(r(i)GA(y/i)TGG

  
  

4516-as

CAGGGCCCCCAT(n/i)GACA

381 bp

45°C

Hex3'-cons

Hexon

4517-s

CGCAATGGTC(n/i)TACATGCAC

  
  

4517-as

CAGTGCCCGA(r/i)TA(k/i)GG(n/i)TT

340 bp

45°C

  

4518-s

GCAGGACGC(y/i)TCGGAGTA

  
  

4518-as

CACCC(k/i)GTT(r/i)TC(n/i)CC

230 bp

45°C

pTP-cons

pTP

4521-s

TGGCGACGT(n/i)GT(n/i)TACAG

  
  

4521-as

CGGACT(y/i)(k/i)GA(r/i)CCTGAAA

260 bp

45°C

  

4522-s

TACAGCCG(n/i)GTSTGGAAC

  
  

4522-as

CTGAAAGAGAGTTC(n/i)ACAGAATCA

230 bp

45°C

Specific primers for long-distance PCR

pTP-DPOL-LD

pTP, DPOL

4659-s

TCGCATCTCCAACGACCT

  
  

4659-as

GCATCCATGGTGAAGATTCC

2350 bp

60°C

Hex-LD

Hexon

4618-s

AGTTCGCTACACACTGGCTG

  
  

4618-as

ATTGCGGTGATGATTGAATG

1354 bp

59°C

pTP-Hex-LD

pTP, Hexon

4662-s

CTCGGTATCGTTGACGGC

  
  

4662-as

GATCAACGGGCACAAAGC

10044 bp

60°C

Primers specific for AdV species B

Hex-loop2

Hexon

5442s

GAACAAGATACTTTAGCATGTGGAA

  
  

5442as

GATTGAATGGATTAACATTGTCC

468 bp

55°C

 

Hexon

5443s

TAGAAAATCACGGGGTGGAAGA

  
  

5443as

GGCATCCAAAGACCATCTG

380 bp

55°C

$ s = sense, as = antisense # I = inosine

Table 2

Adenoviruses, accession numbers and hosts

Adenovirus

Abbreviation

GenBank accession number

Host

Wild (Gabon)

Captive

HAdV-B of this study

     

Gorilla gorilla adenovirus B7

GgorAdV-B7

HQ292614

Western lowland gorilla

+

+

Gorilla gorilla adenovirus B8

GgorAdV-B8

HQ292615

Western lowland gorilla

+

+

Gorilla gorilla adenovirus B9

GgorAdV-B9

HQ292616

Western lowland gorilla

 

+

Gorilla gorilla adenovirus B10

GgorAdV-B10

HQ292617

Western lowland gorilla

+

 

Published HAdV-B

     

Simian adenovirus 21

SAdV-21

AC000010

Chimpanzee

 

+

Simian adenovirus 27.1

SAdV-27.1

FJ025909

Chimpanzee

 

+

Simian adenovirus 27.2

SAdV-27.2

FJ025928

Gorilla

 

+

Simian adenovirus 28.1

SAdV-28.1

FJ025914

Chimpanzee

 

+

Simian adenovirus 28.2

SAdV-28.2

FJ025915

Gorilla

 

+

Simian adenovirus 29

SAdV-29

FJ025916

Chimpanzee

 

+

Simian adenovirus 32

SAdV-32

FJ025911

Chimpanzee

 

+

Simian adenovirus 33

SAdV-33

JF025908

Chimpanzee

 

+

Simian adenovirus 35.1

SAdV-35.1

FJ025912

Chimpanzee

 

+

Simian adenovirus 35.2

SAdV-35.2

FJ025910

Bonobo

 

+

Simian adenovirus 41.1

SAdV-41.1

FJ025913

Gorilla

 

+

Simian adenovirus 41.2

SAdV-41.2

FJ025927

Gorilla

 

+

Simian adenovirus 46

SAdV-46

FJ025930

Gorilla

 

+

Simian adenovirus 47

SAdV-47

FJ025929

Gorilla

 

+

Human adenovirus B3

HAdV-B3

DQ086466

Human

  

Human adenovirus B7

HAdV-B7

AC000018

Human

  

Human adenovirus B11

HAdV-B11

AY163756

Human

  

Human adenovirus B14

HAdV-B14

AY803294

Human

  

Human adenovirus B16

HAdV-B16

AY601636

Human

  

Human adenovirus B21

HAdV-B21

AY601633

Human

  

Human adenovirus B34

HAdV-B34

AY737797

Human

  

Human adenovirus B35

HAdV-B35

AY271307

Human

  

Human adenovirus B50

HAdV-B50

AY737798

Human

  

To acquire extended sequence information of GgorAdV-B7, three additional nested PCR assays were designed (Table 1) targeting the preterminal protein (pTP) and two conserved regions at the 5'- and 3'-end of the hexon gene (Figure 1). PCRs were performed as described above, except that elongation at 72°C was for 1 min. With each primer set products of the expected size were obtained. BLAST analysis of their sequences also revealed a HAdV-B-like virus (not shown). To prove that the DPOL, pTP and hexon sequences originate from the same virus, we connected them with long-distance (LD) PCRs (Figure 1) using the TaKaRa-EX PCR system according to the instructions of the manufacturer (Takara Bio Inc., Otsu, Japan). The LD primer pairs are listed with their annealing temperatures in Table 1. Three overlapping PCR products were generated and sequenced by primer walking. A final contiguous sequence of 15637 bp was obtained spanning the genes DPOL, pTP and 52 k, the genes encoding the AdV proteins pIIIa, III (penton base), pVII, V, pX and pVI, and the hexon gene of GgorAdV-B7 (Figure 1).

Since the AdV hexon gene is an important member of the core gene set used for AdV classification [2, 3, 13, 14], we compared the available partial hexon gene of GgorAdV-B7 (2.7 kb) pair-wise with the corresponding hexon sequences of the most closely related human and chimpanzee HAdV-B viruses and all published gorilla HAdV-B viruses. The highest identity percentages were 96.6% for SAdV-35.1 (chimpanzee AdV) and 96% for HAdV-B21. The gorilla AdV SAdV-27.2, SAdV-28.2, SAdV-41.1, SAdV-41.2, SAdV-46 and SAdV-47 revealed only 87-91% identity. This closer relationship to HAdV-B21 and SAdV-35.1 was restricted to the loop-encoding regions 1 and 2 [15] as visible in an analysis with the software SIMPLOT http://sray.med.som.jhmi.edu (Figure 2). In pair-wise comparisons of DPOL and pTP genes, GgorAdV-B7 was equally closely related to chimpanzee and gorilla HAdV-B viruses (96-99.9%). However, the penton base gene of GgorAdV-B7 showed a striking similarity (99.7%) only to that of SAdV-29 (chimpanzee AdV). Using the program mVISTA http://genome.lbl.gov/vista/index.shtml, the near-perfect match of the GgorAdV-B7 and SAdV-29 penton base genes over the entire gene length is clearly visible (Figure 3).
Figure 2

Simplot analysis of the hexon gene. 2.8 kb of the GgorAdV-B7 hexon gene were compared to the hexon genes of selected chimpanzee (green and red line), gorilla (blue line) and human (yellow and grey line) AdVs. Below the plot, the analysis parameters are listed in blue font. The hexon Loop 1 and Loop 2 regions are indicated at the bottom.

Figure 3

Pairwise sequence alignment of the penton base open reading frame. The penton base gene of GgorAdV-B7 was compared with those of five gorilla-, three chimpanzee- and two human AdVs. The 50-100 percent sequence conservation is represented by the height of each data point along the y axis. The chimpanzee AdV SAdV-29 is highlighted in grey designating the exceptionally high similarity to GgorAdV-B7.

With the PhyML plug-in 2.0.1 of the Geneious Pro 5.0.4 software, phylogenetic trees were constructed on the basis of hexon, DPOL, pTP and penton base gene alignments (Figures 4). All published, completely sequenced HAdV-B viruses were included. In the hexon-based tree, GgorAdV-B7 clustered with HAdV-B21, SAdV-35.1 (chimpanzee AdV) and SAdV-35.2 (bonobo AdV) (Figure 4a). DPOL and pTP analyses placed GgorAdV-B7 into a tight cluster of gorilla and chimpanzee AdVs (Figure 4b and 4c). In the tree derived from the penton base, GgorAdV-B7 branched separately, nearly at the same position as SAdV-29 (Figure 4d). With the MrBayes 2.0.2 plug-in (Geneious Pro) or the Neighbor-Joining module of MacVector 10.6, trees with the same AdV clusters and similarly supported topology were obtained (data not shown).
Figure 4

Phylogenetic analysis. The Hexon (A), DPOL (B), pTP (C) and penton (D) sequences of GgorAdV-B7 and those of published NHP and human HAdV-B viruses were aligned and subjected to phylogenetic analysis. Human, chimpanzee, bonobo and gorilla AdVs are in black, blue, green and red font, respectively. AdVs discovered in this study are marked with black dots.

The remarkably close relatedness of GgorAdV-B7 to chimpanzee AdVs (SAdV-29 and 35.1) prompted us to investigate whether gorillas naturally host GgorAdV-B7. For this purpose, we examined wild Western lowland gorillas (Gorilla. g. gorilla) from Gabon and additional captive gorillas. Fecal samples were collected from 19 individuals in a remote area with little human presence in Loango National Park, Gabon. They originated from fresh nest sites or were freshly found on gorilla paths [16]. Samples were collected using single-use gloves and preserved by drying over silica. DNA was extracted following a previously described method [17]. In addition, ten necropsy samples (spleen, liver, pancreas, lymph node, tonsil, lung, kidney, urine) and one plasma sample were collected from four deceased captive gorillas in the Zoological gardens of Berlin as well as six fecal samples from three captive gorillas in the Zoological gardens of Münster, Germany. To test for the presence of HAdV-B viruses, we set up a nested PCR (PCR Hex-loop2; Table 1) which targets flanking sequences of a hyper variable region (loop 2) in the hexon gene (Figure 1) and amplifies 380 bp. The primers were deduced from HAdV-B sequences only and not degenerated. A total of 36 gorilla samples were screened. AdV DNA was only detected in feces (5/19 wild gorilla samples and 4/6 captive gorilla samples). In total, 9/25 fecal samples were PCR-positive (36%), and the products sequenced. Most importantly, a virus apparently identical to GgorAdV-B7 was identified in a wild gorilla from Gabon. Three additional HAdV-B viruses were also detected. Two were without close similarities to any published AdV sequence. The third one was nearly identical to the gorilla AdVs SAdV-27.2 and SAdV-47, which had been originally isolated from captive individuals [12]. They were tentatively named GgorAdV-B8, -B9 and -B10.

GgorAdV-B8 was detected in two fecal samples from wild gorillas in Gabon and in one sample from Münster. Its hexon sequence revealed the highest percentage of identity (86.5%) to SAdV-21 (chimpanzee HAdV-B). GgorAdV-B9 was only amplified from captive gorillas (two fecal samples from Münster) and showed 88% identity to SAdV-29 (chimpanzee HAdV-B). The GgorAdV-B7 to -B10 Hex-loop2 sequences and closely related sequences of published gorilla, chimpanzee, bonobo and human HAdV-B viruses were subjected to phylogenetic analysis as described above. In the tree, the HAdV-B viruses segregate into several subclades with members of two, three or four host species (human, chimpanzee, bonobo and gorilla) (Figure 5). This mixed clustering was also observed upon analysis of the nearly complete hexon gene (2.7 kb; Figure 4a) with GgorAdV-B7 only. It was partially visible in the penton base tree (Figure 4d) and entirely absent from the DPOL and pTP trees (Figures 4b and 4c). In addition, the phylogenetic position of a given primate AdV frequently differed, depending on the analyzed gene (compare Figures 4a to 4d).
Figure 5

Phylogenetic analysis of the hexon loop 2 region. For details, see legend of Figure 4.

Taken together, these observations cannot be explained by co-speciation. Rather, they are in line with recombination and host switching. Such events have been previously discussed to be involved in the evolution of human AdV, because intra-species shuffling of penton base, fiber and hexon genes has been frequently observed [46]. In addition, a recombinant between viruses of the sub-clades HAdV-B1 and HAdV-B2 has been isolated from a captive chimpanzee [12]. Here, a close similarity of GgorAdV-B7 to SAdV-29 (complete sequence, excluding hexon loops) and to SAdV-35.1 (hexon loops) was observed (Figure 2). However, since in the loop region the nucleic acid identity between GgorAdV-B7 and SAdV-35.1 was well below 100%, it is unlikely that the existing AdVs are parent viruses in a recent recombination event giving rise to GgorAdV-B7. Rather, a more ancient one with subsequent genetic drift may have been involved or recombination with an unknown AdV, as suggested for HAdV-A18 [18].

Shuffling of genes by recombination between AdVs that naturally infect different host species (e.g., great ape and human AdVs) but under certain conditions co-infect the same host, may be an additional mechanism by which AdVs exchange genetic information. This could occur in places where contacts between humans and apes are frequent like in zoos and animal facilities. In addition, people who are involved in hunting primates and preparation of bush meat [19] are at risk to be infected. So far, infections of humans with non-human primate (NHP) AdVs have not been observed. Nevertheless, antibodies with specificity for chimpanzee HAdV-C viruses have been detected in humans from Sub-Saharan Africa and were significantly less frequent in people from the United States of America and Thailand [20]. In addition, the species HAdV-E comprises only one human serotype but more than 12 great ape serotypes. Therefore, the human HAdV-E was thought to be the result of a zoonotic transmission from chimpanzees to humans [21]. The gorilla AdV described in the present study (GgorAdV-B7) is highly similar to chimpanzee AdVs. Thus, a transmission event between chimpanzees and gorillas was possibly involved which is further indication for the potential of AdVs to jump between closely related hosts.

Very little is known about the pathogenic properties of NHP-AdV. GgorAdV-B7 was originally discovered in a group of gorillas suffering from prolonged diarrhea and self-limiting respiratory infection. Since human species B AdV have been linked to respiratory diseases [2224], an etiological association of GgorAdV-B7 with the observed respiratory symptoms is possible. However, recent studies reported the frequent shedding of AdVs in the feces of healthy captive chimpanzees and gorillas [12, 25]. Therefore, further investigations are needed.

Knowledge about the spectrum of AdV in wild great apes in general [25] is very limited. Specifically from wild gorillas, no information has been published. Although examining only a small set of samples, our findings show that AdV infecting captive gorillas can readily be found in wild animals (GgorAdV-B7; GgorAdV-B8). This is a good example of how humans may be brought into contact with new pathogens, not only locally through bushmeat hunting in regions where NHP live naturally, but also in other regions of the world where NHP are housed in zoos.

The high variety of known and novel HAdV-B viruses in great apes calls for larger studies to understand the diversity of AdVs currently circulating in African NHP as well as in local human populations. It is justified to assume that such studies will improve our insight into the zoonotic potential of adenoviruses and possibly answer the intriguing question whether AdVs of non-human primates have already contributed to the human "adeno-virosphere".

Accession numbers

The sequences reported in this study were deposited in GenBank under the accession numbers listed in Table 2.

Declarations

Acknowledgements

We thank Michael Laue for electron microscopic analysis. The technical assistance of Sonja Liebmann and Cornelia Walter is kindly acknowledged. We thank the Agence Nationale des Parcs Nationaux (ANPN) and the Centre National de la Recherche Scientifique et Technique (CENAREST) of Gabon for permission to conduct research in Loango National Park. We also thank the Société pour la Conservation et le Développement (SCD) and Wildlife Conservation Society (WCS) for financial and logistical support. For sample collection from wild gorilla, we thank L. Rabanal, L. Mackaga, E. R. Guizard, N. Tagg, B. Graw, E. Fairet, M. Gregoire, L. Rankin and the other field assistants of the Loango Ape project. For DNA extraction and identification of individual samples from wild gorilla we thank M. Arandjelovic and L. Vigilant from the Max-Planck-Institute for Evolutionary Anthropology, Leipzig.

Authors’ Affiliations

(1)
FG12 Division of Viral Infections, Robert Koch Institute
(2)
Junior research group "Emerging Zoonoses", Robert Koch Institute
(3)
Department of Primatology, Max-Planck-Institute for Evolutionary Anthropology
(4)
Westfälischer Zoologischer Garten Münster GmbH
(5)
Institute of Medical Microbiology, Clinical Virology, University of Münster

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© Wevers et al; licensee BioMed Central Ltd. 2010

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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