Publications by authors named "Sébastien Calvignac-Spencer"

72 Publications

Discovery of novel herpes simplexviruses in wild gorillas, bonobos, and chimpanzees supports zoonotic origin of HSV-2.

Mol Biol Evol 2021 Mar 15. Epub 2021 Mar 15.

Viral Evolution, Robert Koch Institute, Berlin, Germany.

Viruses closely related to human pathogens can reveal the origins of human infectious diseases. Human herpes simplexvirus type 1 (HSV-1) and type 2 (HSV-2) are hypothesized to have arisen via host-virus co-divergence and cross-species transmission. We report the discovery of novel herpes simplexviruses during a large-scale screening of fecal samples from wild gorillas, bonobos, and chimpanzees. Phylogenetic analysis indicates that, contrary to expectation, simplexviruses from these African apes are all more closely related to HSV-2 than to HSV-1. Molecular clock-based hypothesis testing suggests the divergence between HSV-1 and the African great ape simplexviruses likely represents a codivergence event between humans and gorillas. The simplexviruses infecting African great apes subsequently experienced multiple cross-species transmission events over the past 3 million years, the most recent of which occurred between humans and bonobos around 1 million years ago. These findings revise our understanding of the origins of human herpes simplexviruses and suggest that HSV-2 is one of the earliest zoonotic pathogens.
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http://dx.doi.org/10.1093/molbev/msab072DOI Listing
March 2021

Risk of human-to-wildlife transmission of SARS-CoV-2.

Mamm Rev 2020 Oct 6. Epub 2020 Oct 6.

Department of Biology University of Antwerp Universiteitsplein 1 Antwerp 2610 Belgium.

It has been a long time since the world has experienced a pandemic with such a rapid devastating impact as the current COVID-19 pandemic. The causative agent, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), is unusual in that it appears capable of infecting many different mammal species. As a significant proportion of people worldwide are infected with SARS-CoV-2 and may spread the infection unknowingly before symptoms occur or without any symptoms ever occurring, there is a non-negligible risk of humans spreading SARS-CoV-2 to wildlife, in particular to wild non-human mammals. Because of SARS-CoV-2's apparent evolutionary origins in bats and reports of humans transmitting the virus to pets and zoo animals, regulations for the prevention of human-to-animal transmission have so far focused mostly on these animal groups. We summarise recent studies and reports that show that a wide range of distantly related mammals are likely to be susceptible to SARS-CoV-2, and that susceptibility or resistance to the virus is, in general, not predictable, or only predictable to some extent, from phylogenetic proximity to known susceptible or resistant hosts. In the absence of solid evidence on the susceptibility and resistance to SARS-CoV-2 for each of the >6500 mammal species, we argue that sanitary precautions should be taken by humans interacting with any other mammal species in the wild. Preventing human-to-wildlife SARS-CoV-2 transmission is important to protect these animals (some of which are classed as threatened) from disease, but also to avoid establishment of novel SARS-CoV-2 reservoirs in wild mammals. The risk of repeated re-infection of humans from such a wildlife reservoir could severely hamper SARS-CoV-2 control efforts. Activities during which direct or indirect interaction with wild mammals may occur include wildlife research, conservation activities, forestry work, pest control, management of feral populations, ecological consultancy work, management of protected areas and natural environments, wildlife tourism and wildlife rehabilitation in animal shelters. During such activities, we recommend sanitary precautions, such as physical distancing, wearing face masks and gloves, and frequent decontamination, which are very similar to regulations currently imposed to prevent transmission among humans. We further recommend active surveillance of domestic and feral animals that could act as SARS-CoV-2 intermediate hosts between humans and wild mammals.
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http://dx.doi.org/10.1111/mam.12225DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7675675PMC
October 2020

Comparison of target enrichment strategies for ancient pathogen DNA.

Biotechniques 2020 12 2;69(6):455-459. Epub 2020 Nov 2.

Institute for Archaeological Sciences, Archaeo- & Palaeogenetics, University of Tübingen, 72070 Tübingen, Germany.

In ancient DNA research, the degraded nature of the samples generally results in poor yields of highly fragmented DNA; targeted DNA enrichment is thus required to maximize research outcomes. The three commonly used methods - array-based hybridization capture and in-solution capture using either RNA or DNA baits - have different characteristics that may influence the capture efficiency, specificity and reproducibility. Here we compare their performance in enriching pathogen DNA of and from 11 ancient and 19 modern samples. We find that in-solution approaches are the most effective method in ancient and modern samples of both pathogens and that RNA baits usually perform better than DNA baits.
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http://dx.doi.org/10.2144/btn-2020-0100DOI Listing
December 2020

Geographically structured genomic diversity of non-human primate-infecting subsp. .

Microb Genom 2020 11;6(11)

Viral Evolution, Robert Koch Institute, Berlin, Germany.

Many non-human primate species in sub-Saharan Africa are infected with subsp. , the bacterium causing yaws in humans. In humans, yaws is often characterized by lesions of the extremities and face, while subsp. causes venereal syphilis and is typically characterized by primary lesions on the genital, anal or oral mucosae. It remains unclear whether other subspecies found in humans also occur in non-human primates and how the genomic diversity of non-human primate subsp. lineages is distributed across hosts and space. We observed orofacial and genital lesions in sooty mangabeys () in Taï National Park, Côte d'Ivoire and collected swabs and biopsies from symptomatic animals. We also collected non-human primate bones from 8 species in Taï National Park and 16 species from 11 other sites across sub-Saharan Africa. Samples were screened for DNA using polymerase chain reactions (PCRs) and we used in-solution hybridization capture to sequence genomes. We generated three nearly complete genomes from biopsies and swabs and detected treponemal DNA in bones of six non-human primate species in five countries, allowing us to reconstruct three partial genomes. Phylogenomic analyses revealed that both orofacial and genital lesions in sooty mangabeys from Taï National Park were caused by subsp. . We showed that subsp. has infected non-human primates in Taï National Park for at least 28 years and has been present in two non-human primate species that had not been described as subsp. hosts in this ecosystem, western chimpanzees () and western red colobus (), complementing clinical evidence that started accumulating in Taï National Park in 2014. More broadly, simian subsp. strains did not form monophyletic clades based on host species or the symptoms caused, but rather clustered based on geography. Geographical clustering of subsp. genomes might be compatible with cross-species transmission of subsp. within ecosystems or environmental exposure, leading to the acquisition of closely related strains. Finally, we found no evidence for mutations that confer antimicrobial resistance.
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http://dx.doi.org/10.1099/mgen.0.000463DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7725339PMC
November 2020

Molecular epidemiological typing of isolates identifies a novel association between genogroup G10557 (G7072) and decreased susceptibility to cefixime, Germany, 2014 to 2017.

Euro Surveill 2020 10;25(41)

The members of the GORENET study group are acknowledged at the end of the article.

BackgroundEmerging antimicrobial resistance (AMR) challenges gonorrhoea treatment and requires surveillance.AimThis observational study describes the genetic diversity of isolates in Germany from 2014 to 2017 and identifies multi-antigen sequence typing (NG-MAST) genogroups associated with AMR or some patient demographics.Methods1,220 gonococcal isolates underwent AMR testing and NG-MAST. Associations between genogroups and AMR or sex/age of patients were statistically assessed.ResultsPatients' median age was 32 years (interquartile range: 25-44); 1,078 isolates (88.4%) originated from men. In total, 432 NG-MAST sequence types including 156 novel ones were identified, resulting in 17 major genogroups covering 59.1% (721/1,220) of all isolates. Genogroups G1407 and G10557 (G7072) were significantly associated with decreased susceptibility to cefixime (Kruskal-Wallis chi-squared: 549.3442, df: 16, p < 0.001). Their prevalences appeared to decline during the study period from 14.2% (15/106) to 6.2% (30/481) and from 6.6% (7/106) to 3.1% (15/481) respectively. Meanwhile, several cefixime susceptible genogroups' prevalence seemed to increase. Proportions of isolates from men differed among genogroups (Fisher's exact test, p < 0.001), being e.g. lower for G25 (G51) and G387, and higher for G5441 and G2992. Some genogroups differed relative to each other in affected patients' median age (Kruskal-Wallis chi-squared:  47.5358, df:  16, p < 0.001), with e.g. G25 (G51) and G387 more frequent among ≤ 30 year olds and G359 and G17420 among ≥ 40 year olds.ConclusionAMR monitoring with molecular typing is important. Dual therapy (ceftriaxone plus azithromycin) recommended in 2014 in Germany, or only the ceftriaxone dose of this therapy, might have contributed to cefixime-resistant genogroups decreasing.
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http://dx.doi.org/10.2807/1560-7917.ES.2020.25.41.1900648DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7565851PMC
October 2020

Identification of African swine fever virus-like elements in the soft tick genome provides insights into the virus' evolution.

BMC Biol 2020 10 8;18(1):136. Epub 2020 Oct 8.

Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Südufer 10, 17493, Greifswald-Insel Riems, Germany.

Background: African swine fever virus (ASFV) is a most devastating pathogen affecting swine. In 2007, ASFV was introduced into Eastern Europe where it continuously circulates and recently reached Western Europe and Asia, leading to a socio-economic crisis of global proportion. In Africa, where ASFV was first described in 1921, it is transmitted between warthogs and soft ticks of the genus Ornithodoros in a so-called sylvatic cycle. However, analyses into this virus' evolution are aggravated by the absence of any closely related viruses. Even ancient endogenous viral elements, viral sequences integrated into a host's genome many thousand years ago that have proven extremely valuable to analyse virus evolution, remain to be identified. Therefore, the evolution of ASFV, the only known DNA virus transmitted by arthropods, remains a mystery.

Results: For the identification of ASFV-like sequences, we sequenced DNA from different recent Ornithodoros tick species, e.g. O. moubata and O. porcinus, O. moubata tick cells and also 100-year-old O. moubata and O. porcinus ticks using high-throughput sequencing. We used BLAST analyses for the identification of ASFV-like sequences and further analysed the data through phylogenetic reconstruction and molecular clock analyses. In addition, we performed tick infection experiments as well as additional small RNA sequencing of O. moubata and O. porcinus soft ticks.

Conclusion: Here, we show that soft ticks of the Ornithodoros moubata group, the natural arthropod vector of ASFV, harbour African swine fever virus-like integrated (ASFLI) elements corresponding to up to 10% (over 20 kb) of the ASFV genome. Through orthologous dating and molecular clock analyses, we provide data suggesting that integration could have occurred over 1.47 million years ago. Furthermore, we provide data showing ASFLI-element specific siRNA and piRNA in ticks and tick cells allowing for speculations on a possible role of ASFLI-elements in RNA interference-based protection against ASFV in ticks. We suggest that these elements, shaped through many years of co-evolution, could be part of an evolutionary virus-vector 'arms race', a finding that has not only high impact on our understanding of the co-evolution of viruses with their hosts but also provides a glimpse into the evolution of ASFV.
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http://dx.doi.org/10.1186/s12915-020-00865-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7542975PMC
October 2020

Multiple DNA viruses identified in multimammate mouse (Mastomys natalensis) populations from across regions of sub-Saharan Africa.

Arch Virol 2020 Oct 4;165(10):2291-2299. Epub 2020 Aug 4.

Division 12 "Measles, Mumps, Rubella, and Viruses Affecting Immunocompromised Patients", Robert Koch Institut, Berlin, Germany.

The multimammate mouse (Mastomys natalensis; M. natalensis) serves as the main reservoir for the zoonotic arenavirus Lassa virus (LASV), and this has led to considerable investigation into the distribution of LASV and other related arenaviruses in this host species. In contrast to the situation with arenaviruses, the presence of other viruses in M. natalensis remains largely unexplored. In this study, herpesviruses and polyomaviruses were identified and partially characterized by PCR methods, sequencing, and phylogenetic analysis. In tissues sampled from M. natalensis populations in Côte d'Ivoire and Mali, six new DNA viruses (four betaherpesviruses, one gammaherpesvirus and one polyomavirus) were identified. Phylogenetic analysis based on glycoprotein B amino acid sequences showed that the herpesviruses clustered with cytomegaloviruses and rhadinoviruses of multiple rodent species. The complete circular genome of the newly identified polyomavirus was amplified by PCR. Amino acid sequence analysis of the large T antigen or VP1 showed that this virus clustered with a known polyomavirus from a house mouse (species Mus musculus polyomavirus 1). These two polyomaviruses form a clade with other rodent polyomaviruses, and the newly identified virus represents the third known polyomavirus of M. natalensis. This study represents the first identification of herpesviruses and the discovery of a novel polyomavirus in M. natalensis. In contrast to arenaviruses, we anticipate that these newly identified viruses represent a low zoonotic risk due to the normally highly restricted specificity of members of these two DNA virus families to their individual mammalian host species.
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http://dx.doi.org/10.1007/s00705-020-04738-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7497350PMC
October 2020

Measles virus and rinderpest virus divergence dated to the sixth century BCE.

Science 2020 06;368(6497):1367-1370

Epidemiology of Highly Pathogenic Microorganisms Project Group, Robert Koch Institute, Berlin, Germany.

Many infectious diseases are thought to have emerged in humans after the Neolithic revolution. Although it is broadly accepted that this also applies to measles, the exact date of emergence for this disease is controversial. We sequenced the genome of a 1912 measles virus and used selection-aware molecular clock modeling to determine the divergence date of measles virus and rinderpest virus. This divergence date represents the earliest possible date for the establishment of measles in human populations. Our analyses show that the measles virus potentially arose as early as the sixth century BCE, possibly coinciding with the rise of large cities.
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http://dx.doi.org/10.1126/science.aba9411DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7713999PMC
June 2020

Encodes a Bacterium-like 2,4-Dienoyl-Coenzyme A Reductase That Is Required for Fatty Acid β-Oxidation and Intracellular Parasite Survival.

mBio 2020 06 2;11(3). Epub 2020 Jun 2.

Mycotic and Parasitic Agents and Mycobacteria (FG16), Department of Infectious Diseases, Robert Koch Institute, Berlin, Germany

spp. are protozoan parasites that cause a spectrum of important diseases in humans. These parasites develop as extracellular promastigotes in the digestive tract of their insect vectors and as obligate intracellular amastigotes that infect macrophages and other phagocytic cells in their vertebrate hosts. Promastigote-to-amastigote differentiation is associated with marked changes in metabolism, including the upregulation of enzymes involved in fatty acid β-oxidation, which may reflect adaptation to the intracellular niche. Here, we have investigated the function of one of these enzymes, a putative 2,4-dienoyl-coenzyme A (CoA) reductase (DECR), which is specifically required for the β-oxidation of polyunsaturated fatty acids. The DECR shows close homology to bacterial DECR proteins, suggesting that it was acquired by lateral gene transfer. It is present in other trypanosomatids that have obligate intracellular stages (i.e., and ) but is absent from dixenous parasites with an exclusively extracellular lifestyle (i.e., ). A DECR-green fluorescent protein (GFP) fusion protein was localized to the mitochondrion in both promastigote and amastigote stages, and the levels of expression increased in the latter stages. A Δ null mutant was unable to catabolize unsaturated fatty acids and accumulated the intermediate 2,4-decadienoyl-CoA, confirming DECR's role in β-oxidation. Strikingly, the Δ mutant was unable to survive in macrophages and was avirulent in BALB/c mice. These findings suggest that β-oxidation of polyunsaturated fatty acids is essential for intracellular parasite survival and that the bacterial origin of key enzymes in this pathway could be exploited in developing new therapies. The Trypanosomatidae are protozoan parasites that infect insects, plants, and animals and have evolved complex monoxenous (single host) and dixenous (two hosts) lifestyles. A number of species of Trypanosomatidae, including spp., have evolved the capacity to survive within intracellular niches in vertebrate hosts. The adaptations, metabolic and other, that are associated with development of intracellular lifestyles remain poorly defined. We show that genomes of and Trypanosomatidae that can survive intracellularly encode a 2,4-dienoyl-CoA reductase that is involved in catabolism of a subclass of fatty acids. The trypanosomatid enzyme shows closest similarity to the corresponding bacterial enzymes and is located in the mitochondrion and essential for intracellular growth of The findings suggest that acquisition of this gene by lateral gene transfer from bacteria by ancestral monoxenous Trypanosomatidae likely contributed to the development of a dixenous lifestyle of these parasites.
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http://dx.doi.org/10.1128/mBio.01057-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7267886PMC
June 2020

Author Correction: Evidence for Human Streptococcus pneumoniae in wild and captive chimpanzees: A potential threat to wild populations.

Sci Rep 2020 May 29;10(1):9062. Epub 2020 May 29.

Epidemiology of highly pathogenic microorganisms, Robert Koch-Institute, 13353, Berlin, Germany.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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http://dx.doi.org/10.1038/s41598-020-66183-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7260240PMC
May 2020

Yaws Disease Caused by Treponema pallidum subspecies pertenue in Wild Chimpanzee, Guinea, 2019.

Emerg Infect Dis 2020 06;26(6):1283-1286

Yaws-like lesions are widely reported in wild African great apes, yet the causative agent has not been confirmed in affected animals. We describe yaws-like lesions in a wild chimpanzee in Guinea for which we demonstrate infection with Treponema pallidum subsp. pertenue. Assessing the conservation implications of this pathogen requires further research.
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http://dx.doi.org/10.3201/eid2606.191713DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7258472PMC
June 2020

Monkeypox virus emergence in wild chimpanzees reveals distinct clinical outcomes and viral diversity.

Nat Microbiol 2020 07 27;5(7):955-965. Epub 2020 Apr 27.

Project Group Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, Berlin, Germany.

Monkeypox is a viral zoonotic disease on the rise across endemic habitats. Despite the growing importance of monkeypox virus, our knowledge on its host spectrum and sylvatic maintenance is limited. Here, we describe the recent repeated emergence of monkeypox virus in a wild, human-habituated western chimpanzee (Pan troglodytes verus, hereafter chimpanzee) population from Taï National Park, Ivory Coast. Through daily monitoring, we show that further to causing its typical exanthematous syndrome, monkeypox can present itself as a severe respiratory disease without a diffuse rash. By analysing 949 non-invasively collected samples, we identify the circulation of at least two distinct monkeypox virus lineages and document the shedding of infectious particles in faeces and flies, suggesting that they could mediate indirect transmission. We also show that the carnivorous component of the Taï chimpanzees' diet, mainly consisting of the sympatric monkeys they regularly hunt, did not change nor shift towards rodent consumption (the presumed reservoir) before the outbreaks, suggesting that the sudden emergence of monkeypox virus in this population is probably due to changes in the ecology of the virus itself. Using long-term mortality surveillance data from Taï National Park, we provide evidence of little to no prior viral activity over at least two decades. We conclude that great ape sentinel systems devoted to the longitudinal collection of behavioural and health data can help clarify the epidemiology and clinical presentation of zoonotic pathogens.
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http://dx.doi.org/10.1038/s41564-020-0706-0DOI Listing
July 2020

Search for polyoma-, herpes-, and bornaviruses in squirrels of the family Sciuridae.

Virol J 2020 03 27;17(1):42. Epub 2020 Mar 27.

Division 12 'Measles, Mumps, Rubella and Viruses Affecting Immunocompromised Patients', Robert Koch-Institute, Berlin, Germany.

Background: Squirrels (family Sciuridae) are globally distributed members of the order Rodentia with wildlife occurrence in indigenous and non-indigenous regions (as invasive species) and frequent presence in zoological gardens and other holdings. Multiple species introductions, strong inter-species competition as well as the recent discovery of a novel zoonotic bornavirus resulted in increased research interest on squirrel pathogens. Therefore we aimed to test a variety of squirrel species for representatives of three virus families.

Methods: Several species of the squirrel subfamilies Sciurinae, Callosciurinae and Xerinae were tested for the presence of polyomaviruses (PyVs; family Polyomaviridae) and herpesviruses (HVs; family Herpesviridae), using generic nested polymerase chain reaction (PCR) with specificity for the PyV VP1 gene and the HV DNA polymerase (DPOL) gene, respectively. Selected animals were tested for the presence of bornaviruses (family Bornaviridae), using both a broad-range orthobornavirus- and a variegated squirrel bornavirus 1 (VSBV-1)-specific reverse transcription-quantitative PCR (RT-qPCR).

Results: In addition to previously detected bornavirus RNA-positive squirrels no more animals tested positive in this study, but four novel PyVs, four novel betaherpesviruses (BHVs) and six novel gammaherpesviruses (GHVs) were identified. For three PyVs, complete genomes could be amplified with long-distance PCR (LD-PCR). Splice sites of the PyV genomes were predicted in silico for large T antigen, small T antigen, and VP2 coding sequences, and experimentally confirmed in Vero and NIH/3T3 cells. Attempts to extend the HV DPOL sequences in upstream direction resulted in contiguous sequences of around 3.3 kilobase pairs for one BHV and two GHVs. Phylogenetic analysis allocated the novel squirrel PyVs to the genera Alpha- and Betapolyomavirus, the BHVs to the genus Muromegalovirus, and the GHVs to the genera Rhadinovirus and Macavirus.

Conclusions: This is the first report on molecular identification and sequence characterization of PyVs and HVs and the detection of bornavirus coinfections with PyVs or HVs in two squirrel species. Multiple detection of PyVs and HVs in certain squirrel species exclusively indicate their potential host association to a single squirrel species. The novel PyVs and HVs might serve for a better understanding of virus evolution in invading host species in the future.
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http://dx.doi.org/10.1186/s12985-020-01310-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7099801PMC
March 2020

Games academics play and their consequences: how authorship, -index and journal impact factors are shaping the future of academia.

Proc Biol Sci 2019 12 4;286(1916):20192047. Epub 2019 Dec 4.

Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, P.O. Box 1066, Blindern, 0316 Oslo, Norway.

Research is a highly competitive profession where evaluation plays a central role; journals are ranked and individuals are evaluated based on their publication number, the number of times they are cited and their -index. Yet such evaluations are often done in inappropriate ways that are damaging to individual careers, particularly for young scholars, and to the profession. Furthermore, as with all indices, people can play games to better their scores. This has resulted in the incentive structure of science increasingly mimicking economic principles, but rather than a monetary gain, the incentive is a higher score. To ensure a diversity of cultural perspectives and individual experiences, we gathered a team of academics in the fields of ecology and evolution from around the world and at different career stages. We first examine how authorship, -index of individuals and journal impact factors are being used and abused. Second, we speculate on the consequences of the continued use of these metrics with the hope of sparking discussions that will help our fields move in a positive direction. We would like to see changes in the incentive systems, rewarding quality research and guaranteeing transparency. Senior faculty should establish the ethical standards, mentoring practices and institutional evaluation criteria to create the needed changes.
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http://dx.doi.org/10.1098/rspb.2019.2047DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6939250PMC
December 2019

Novel Polyomaviruses in Mammals from Multiple Orders and Reassessment of Polyomavirus Evolution and Taxonomy.

Viruses 2019 10 10;11(10). Epub 2019 Oct 10.

P3 "Viral Evolution", Robert Koch Institute, 13353 Berlin, Germany.

As the phylogenetic organization of mammalian polyomaviruses is complex and currently incompletely resolved, we aimed at a deeper insight into their evolution by identifying polyomaviruses in host orders and families that have either rarely or not been studied. Sixteen unknown and two known polyomaviruses were identified in animals that belong to 5 orders, 16 genera, and 16 species. From 11 novel polyomaviruses, full genomes could be determined. Splice sites were predicted for large and small T antigen (LTAg, STAg) coding sequences (CDS) and examined experimentally in transfected cell culture. In addition, splice sites of seven published polyomaviruses were analyzed. Based on these data, LTAg and STAg annotations were corrected for 10/86 and 74/86 published polyomaviruses, respectively. For 25 polyomaviruses, a spliced middle T CDS was observed or predicted. Splice sites that likely indicate expression of additional, alternative T antigens, were experimentally detected for six polyomaviruses. In contrast to all other mammalian polyomaviruses, three closely related cetartiodactyl polyomaviruses display two introns within their LTAg CDS. In addition, the VP2 of Glis glis (edible dormouse) polyomavirus 1 was observed to be encoded by a spliced transcript, a unique experimental finding within the family. Co-phylogenetic analyses based on LTAg CDS revealed a measurable signal of codivergence when considering all mammalian polyomaviruses, most likely driven by relatively recent codivergence events. Lineage duplication was the only other process whose influence on polyomavirus evolution was unambiguous. Finally, our analyses suggest that an update of the taxonomy of the family is required, including the creation of novel genera of mammalian and non-mammalian polyomaviruses.
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http://dx.doi.org/10.3390/v11100930DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6833039PMC
October 2019

Detection of possible spillover of a novel hantavirus in a Natal mastomys from Guinea.

Virus Genes 2020 Feb 25;56(1):95-98. Epub 2019 Oct 25.

Robert Koch Institut, Berlin, Germany.

To date, only two rodent-borne hantaviruses have been detected in sub-Saharan Africa. Here, we report the detection of a yet unknown hantavirus in a Natal mastomys (Mastomys natalensis) in Méliandou, Guinea, in 2014. The phylogenetic placement of this virus suggests that it might represent a cross-order spillover event from an unknown bat or eulipotyphlan host.
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http://dx.doi.org/10.1007/s11262-019-01709-4DOI Listing
February 2020

Metabarcoding of eukaryotic parasite communities describes diverse parasite assemblages spanning the primate phylogeny.

Mol Ecol Resour 2020 Jan 4;20(1):204-215. Epub 2019 Nov 4.

Primate Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research, Goettingen, Germany.

Despite their ubiquity, in most cases little is known about the impact of eukaryotic parasites on their mammalian hosts. Comparative approaches provide a powerful method to investigate the impact of parasites on host ecology and evolution, though two issues are critical for such efforts: controlling for variation in methods of identifying parasites and incorporating heterogeneity in sampling effort across host species. To address these issues, there is a need for standardized methods to catalogue eukaryotic parasite diversity across broad phylogenetic host ranges. We demonstrate the feasibility of a metabarcoding approach for describing parasite communities by analysing faecal samples from 11 nonhuman primate species representing divergent lineages of the primate phylogeny and the full range of sampling effort (i.e. from no parasites reported in the literature to the best-studied primates). We detected a number of parasite families and regardless of prior sampling effort, metabarcoding of only ten faecal samples identified parasite families previously undescribed in each host (x̅ = 8.5 new families per species). We found more overlap between parasite families detected with metabarcoding and published literature when more research effort-measured as the number of publications-had been conducted on the host species' parasites. More closely related primates and those from the same continent had more similar parasite communities, highlighting the biological relevance of sampling even a small number of hosts. Collectively, results demonstrate that metabarcoding methods are sensitive and powerful enough to standardize studies of eukaryotic parasite communities across host species, providing essential new tools for macroecological studies of parasitism.
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http://dx.doi.org/10.1111/1755-0998.13101DOI Listing
January 2020

Cytomegalovirus distribution and evolution in hominines.

Virus Evol 2019 Jul 1;5(2):vez015. Epub 2019 Aug 1.

Epidemiology of highly pathogenic microorganisms, Robert Koch Institute, Berlin, Germany.

Herpesviruses are thought to have evolved in very close association with their hosts. This is notably the case for cytomegaloviruses (CMVs; genus ) infecting primates, which exhibit a strong signal of co-divergence with their hosts. Some herpesviruses are however known to have crossed species barriers. Based on a limited sampling of CMV diversity in the hominine (African great ape and human) lineage, we hypothesized that chimpanzees and gorillas might have mutually exchanged CMVs in the past. Here, we performed a comprehensive molecular screening of all 9 African great ape species/subspecies, using 675 fecal samples collected from wild animals. We identified CMVs in eight species/subspecies, notably generating the first CMV sequences from bonobos. We used this extended dataset to test competing hypotheses with various degrees of co-divergence/number of host switches while simultaneously estimating the dates of these events in a Bayesian framework. The model best supported by the data involved the transmission of a gorilla CMV to the panine (chimpanzee and bonobo) lineage and the transmission of a panine CMV to the gorilla lineage prior to the divergence of chimpanzees and bonobos, more than 800,000 years ago. Panine CMVs then co-diverged with their hosts. These results add to a growing body of evidence suggesting that viruses with a double-stranded DNA genome (including other herpesviruses, adenoviruses, and papillomaviruses) often jumped between hominine lineages over the last few million years.
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http://dx.doi.org/10.1093/ve/vez015DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6671425PMC
July 2019

Tropical rainforest flies carrying pathogens form stable associations with social nonhuman primates.

Mol Ecol 2019 09 18;28(18):4242-4258. Epub 2019 Jul 18.

Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, Berlin, Germany.

Living in groups provides benefits but also incurs costs such as attracting disease vectors. For example, synanthropic flies associate with human settlements, and higher fly densities increase pathogen transmission. We investigated whether such associations also exist in highly mobile nonhuman primate (NHP) Groups. We studied flies in a group of wild sooty mangabeys (Cercocebus atys atys) and three communities of wild chimpanzees (Pan troglodytes verus) in Taï National Park, Côte d'Ivoire. We observed markedly higher fly densities within both mangabey and chimpanzee groups. Using a mark-recapture experiment, we showed that flies stayed with the sooty mangabey group for up to 12 days and for up to 1.3 km. We also tested mangabey-associated flies for pathogens infecting mangabeys in this ecosystem, Bacillus cereus biovar anthracis (Bcbva), causing sylvatic anthrax, and Treponema pallidum pertenue, causing yaws. Flies contained treponemal (6/103) and Bcbva (7/103) DNA. We cultured Bcbva from all PCR-positive flies, confirming bacterial viability and suggesting that this bacterium might be transmitted and disseminated by flies. Whole genome sequences of Bcbva isolates revealed a diversity of Bcbva, probably derived from several sources. We conclude that flies actively track mangabeys and carry infectious bacterial pathogens; these associations represent an understudied cost of sociality and potentially expose many social animals to a diversity of pathogens.
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http://dx.doi.org/10.1111/mec.15145DOI Listing
September 2019

A Novel Orthohepadnavirus Identified in a Dead Maxwell's Duiker () in Taï National Park, Côte d'Ivoire.

Viruses 2019 03 19;11(3). Epub 2019 Mar 19.

Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, 13353 Berlin, Germany.

New technologies enable viral discovery in a diversity of hosts, providing insights into viral evolution. We used one such approach, the virome capture sequencing for vertebrate viruses (VirCapSeq-VERT) platform, on 21 samples originating from six dead Maxwell's duikers () from Taï National Park, Côte d'Ivoire. We detected the presence of an orthohepadnavirus in one animal and characterized its 3128 bp genome. The highest viral copy numbers were detected in the spleen, followed by the lung, blood, and liver, with the lowest copy numbers in the kidney and heart; the virus was not detected in the jejunum. Viral copy numbers in the blood were in the range known from humans with active chronic infections leading to liver histolytic damage, suggesting this virus could be pathogenic in duikers, though many orthohepadnaviruses appear to be apathogenic in other hosts, precluding a formal test of this hypothesis. The virus was not detected in 29 other dead duiker samples from the Côte d'Ivoire and Central African Republic, suggesting either a spillover event or a low prevalence in these populations. Phylogenetic analysis placed the virus as a divergent member of the mammalian clade of orthohepadnaviruses, though its relationship to other orthohepadnaviruses remains uncertain. This represents the first orthohepadnavirus described in an artiodactyl. We have tentatively named this new member of the genus (family ), Taï Forest hepadnavirus. Further studies are needed to determine whether it, or some close relatives, are present in a broader range of artiodactyls, including livestock.
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http://dx.doi.org/10.3390/v11030279DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6466360PMC
March 2019

Extensive Serological Survey of Multiple African Nonhuman Primate Species Reveals Low Prevalence of Immunoglobulin G Antibodies to 4 Ebola Virus Species.

J Infect Dis 2019 10;220(10):1599-1608

Recherches Translationelles sur VIH et Maladies Infectieuses/Institut national de la santé et de la recherche médicale, Institut de Recherche pour le Développement and University of Montpellier, France.

Bats are considered a reservoir species for Ebola viruses, but nonhuman primates (NHPs) have represented a source of infection in several outbreaks in humans. Here we report serological screening of blood or fecal samples from monkeys (n = 2322) and apes (n = 2327). Thirty-six NHP species from Cameroon, Democratic Republic of the Congo, and Ivory Coast were tested with a sensitive and specific Luminex-based assay for immunoglobulin G antibodies to 4 Ebola virus species. Using the simultaneous presence of antibodies to nucleoproteins and glycoproteins to define positivity, we showed that specific Ebola virus antibodies are not widespread among NHPs. Only 1 mustached monkey (Cercopithecus cephus) from Cameroon was positive for Sudan ebolavirus. These observations support that NHPs are most likely intermediate hosts for Ebola viruses. With the increasing frequency of Ebola outbreaks, it is crucial to identify the animal reservoir and understand the ecology of Ebola viruses to inform disease control.
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http://dx.doi.org/10.1093/infdis/jiz006DOI Listing
October 2019

Evolutionary history of human revealed by genome-wide analyses of related ape parasites.

Proc Natl Acad Sci U S A 2018 09 20;115(36):E8450-E8459. Epub 2018 Aug 20.

Department of Medicine, University of Pennsylvania, Philadelphia, PA 19104;

Wild-living African apes are endemically infected with parasites that are closely related to human , a leading cause of malaria outside Africa. This finding suggests that the origin of was in Africa, even though the parasite is now rare in humans there. To elucidate the emergence of human and its relationship to the ape parasites, we analyzed genome sequence data of strains infecting six chimpanzees and one gorilla from Cameroon, Gabon, and Côte d'Ivoire. We found that ape and human parasites share nearly identical core genomes, differing by only 2% of coding sequences. However, compared with the ape parasites, human strains of exhibit about 10-fold less diversity and have a relative excess of nonsynonymous nucleotide polymorphisms, with site-frequency spectra suggesting they are subject to greatly relaxed purifying selection. These data suggest that human has undergone an extreme bottleneck, followed by rapid population expansion. Investigating potential host-specificity determinants, we found that ape parasites encode intact orthologs of three reticulocyte-binding protein genes (, , and ), which are pseudogenes in all human strains. However, binding studies of recombinant RBP2e and RBP3 proteins to human, chimpanzee, and gorilla erythrocytes revealed no evidence of host-specific barriers to red blood cell invasion. These data suggest that, from an ancient stock of parasites capable of infecting both humans and apes, a severely bottlenecked lineage emerged out of Africa and underwent rapid population growth as it spread globally.
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http://dx.doi.org/10.1073/pnas.1810053115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6130405PMC
September 2018

Factors influencing bacterial microbiome composition in a wild non-human primate community in Taï National Park, Côte d'Ivoire.

ISME J 2018 10 28;12(10):2559-2574. Epub 2018 Jun 28.

Project Group Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, Seestraße 10, 13353, Berlin, Germany.

Microbiomes impact a variety of processes including a host's ability to access nutrients and maintain health. While host species differences in microbiomes have been described across ecosystems, little is known about how microbiomes assemble, particularly in the ecological and social contexts in which they evolved. We examined gut microbiome composition in nine sympatric wild non-human primate (NHP) species. Despite sharing an environment and interspecific interactions, individuals harbored unique and persistent microbiomes influenced by host species, social group, and parentage, but surprisingly not by social relationships among members of a social group. We found a branching order of host-species networks constructed using the composition of their microbiomes as characters, which was incongruent with known NHP phylogenetic relationships, with chimpanzees (Pan troglodytes verus) sister to colobines, upon which they regularly prey. In contrast to phylogenetic clustering found in all monkey microbiomes, chimpanzee microbiomes were unique in that they exhibited patterns of phylogenetic overdispersion. This reflects unique ecological processes impacting microbiome composition in chimpanzees and future studies will elucidate the aspects of chimpanzee ecology, life history, and physiology that explain their unique microbiome community structure. Our study of contemporaneous microbiomes of all sympatric diurnal NHP in an ecosystem highlights the diverse dispersal routes shaping these complex communities.
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http://dx.doi.org/10.1038/s41396-018-0166-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6154966PMC
October 2018

Human Respiratory Syncytial Virus and Streptococcus pneumoniae Infection in Wild Bonobos.

Ecohealth 2018 06 27;15(2):462-466. Epub 2018 Feb 27.

Epidemiology of Highly Pathogenic Microorganisms, Robert Koch-Institute, Seestr 10, 13353, Berlin, Germany.

Despite being important conservation tools, tourism and research may cause transmission of pathogens to wild great apes. Investigating respiratory disease outbreaks in wild bonobos, we identified human respiratory syncytial virus and Streptococcus pneumoniae as causative agents. A One Health approach to disease control should become part of great ape programs.
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http://dx.doi.org/10.1007/s10393-018-1319-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7087961PMC
June 2018

Seasonal and inter-annual variation of malaria parasite detection in wild chimpanzees.

Malar J 2018 Jan 18;17(1):38. Epub 2018 Jan 18.

Project Group Epidemiology of Highly Pathogenic Microorganisms, Robert Koch-Institut, Seestraße 10, 13353, Berlin, Germany.

Background: Cross-sectional surveys of chimpanzee (Pan troglodytes) communities across sub-Saharan Africa show large geographical variation in malaria parasite (Plasmodium spp.) prevalence. The drivers leading to this apparent spatial heterogeneity may also be temporally dynamic but data on prevalence variation over time are missing for wild great apes. This study aims to fill this fundamental gap.

Methods: Some 681 faecal samples were collected from 48 individuals of a group of habituated chimpanzees (Taï National Park, Côte d'Ivoire) across four non-consecutive sampling periods between 2005 and 2015.

Results: Overall, 89 samples (13%) were PCR-positive for malaria parasite DNA. The proportion of positive samples ranged from 0 to 43% per month and 4 to 27% per sampling period. Generalized Linear Mixed Models detected significant seasonal and inter-annual variation, with seasonal increases during the wet seasons and apparently stochastic inter-annual variation. Younger individuals were also significantly more likely to test positive.

Conclusions: These results highlight strong temporal fluctuations of malaria parasite detection rates in wild chimpanzees. They suggest that the identification of other drivers of malaria parasite prevalence will require longitudinal approaches and caution against purely cross-sectional studies, which may oversimplify the dynamics of this host-parasite system.
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http://dx.doi.org/10.1186/s12936-018-2187-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5774132PMC
January 2018

Blow flies as urban wildlife sensors.

Mol Ecol Resour 2018 May 8;18(3):502-510. Epub 2018 Feb 8.

Epidemiology of Highly Pathogenic Microorganisms, Robert Koch-Institute, Berlin, Germany.

Wildlife detection in urban areas is very challenging. Conventional monitoring techniques such as direct observation are faced with the limitation that urban wildlife is extremely elusive. It was recently shown that invertebrate-derived DNA (iDNA) can be used to assess wildlife diversity in tropical rainforests. Flies, which are ubiquitous and very abundant in most cities, may also be used to detect wildlife in urban areas. In urban ecosystems, however, overwhelming quantities of domestic mammal DNA could completely mask the presence of wild mammal DNA. To test whether urban wild mammals can be detected using fly iDNA, we performed DNA metabarcoding of pools of flies captured in Berlin, Germany, using three combinations of blocking primers. Our results show that domestic animal sequences are, as expected, very dominant in urban environments. Nevertheless, wild mammal sequences can often be retrieved, although they usually only represent a minor fraction of the sequence reads. Fly iDNA metabarcoding is therefore a viable approach for quick scans of urban wildlife diversity. Interestingly, our study also shows that blocking primers can interact with each other in ways that affect the outcome of metabarcoding. We conclude that the use of complex combinations of blocking primers, although potentially powerful, should be carefully planned when designing experiments.
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http://dx.doi.org/10.1111/1755-0998.12754DOI Listing
May 2018

Cytomegaloviruses in a Community of Wild Nonhuman Primates in Taï National Park, Côte D'Ivoire.

Viruses 2017 12 29;10(1). Epub 2017 Dec 29.

Division 12 Measles, Mumps, Rubella and Viruses Affecting Immunocompromised Patients, Robert Koch Institute, Seestrasse 10, 13353 Berlin, Germany.

Cytomegaloviruses (CMVs) are known to infect many mammals, including a number of nonhuman primates (NHPs). However, most data available arose from studies led on captive individuals and little is known about CMV diversity in wild NHPs. Here, we analyzed a community of wild nonhuman primates (seven species) in Taï National Park (TNP), Côte d'Ivoire, with two PCR systems targeting betaherpesviruses. CMV DNA was detected in 17/87 primates (4/7 species). Six novel CMVs were identified in sooty mangabeys, Campbell's monkeys and Diana monkeys, respectively. In 3/17 positive individuals (from three NHP species), different CMVs were co-detected. A major part of the glycoprotein B coding sequences of the novel viruses was amplified and sequenced, and phylogenetic analyses were performed that included three previously discovered CMVs of western red colobus from TNP and published CMVs from other NHP species and geographic locations. We find that, despite this locally intensified sampling, NHP CMVs from TNP are completely host-specific, pinpointing the absence or rarity of cross-species transmission. We also show that on longer timescales the evolution of CMVs is characterized by frequent co-divergence with their hosts, although other processes, including lineage duplication and host switching, also have to be invoked to fully explain their evolutionary relationships.
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http://dx.doi.org/10.3390/v10010011DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5795424PMC
December 2017