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Virome Heterogeneity and Connectivity in Waterfowl and Shorebird bioRxiv preprint doi: https://doi.org/10.1101/528174; this version posted January 29, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Virome heterogeneity and connectivity in waterfowl and shorebird 2 communities 3 4 Running Title: Viromes of waterbird communities 5 6 Michelle Wille1*, Mang Shi2, Marcel Klaassen3, Aeron C. Hurt1, Edward C. Holmes2* 7 8 9 1WHO Collaborating Centre for Reference and Research on Influenza, at The Peter Doherty Institute 10 for Infection and Immunity, Melbourne, Australia. 11 2Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of 12 Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, 13 Australia. 14 3Centre for Integrative Ecology, Deakin University, Geelong, Australia. 15 16 *Corresponding author: 17 Michelle Wille [email protected], +61 3 9342 9318 18 Edward C. Holmes [email protected], +61 2 9351 5591 19 1 bioRxiv preprint doi: https://doi.org/10.1101/528174; this version posted January 29, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 20 Abstract 21 Models of host-microbe dynamics typically assume a single-host population infected by a single 22 pathogen. In reality, many hosts form multi-species aggregations and may be infected with an 23 assemblage of pathogens. We used a meta-transcriptomic approach to characterize the viromes of 24 nine avian species in the Anseriformes (ducks) and Charadriiformes (shorebirds). This revealed the 25 presence of 27 viral species, of which 24 were novel, including double-stranded RNA viruses 26 (Picobirnaviridae and Reoviridae), single-stranded RNA viruses (Astroviridae, Caliciviridae, 27 Picornaviridae), a retro-transcribing DNA virus (Hepadnaviridae), and a single-stranded DNA virus 28 (Parvoviridae). These viruses comprise multi-host generalist viruses and those that are host-specific, 29 indicative of both virome connectivity and heterogeneity. Virome connectivity was apparent in two 30 well described multi-host virus species (avian coronavirus and influenza A virus) and a novel 31 Rotavirus species that were shared among some Anseriform species, while heterogeneity was 32 reflected in the absence of viruses shared between Anseriformes and Charadriiformes. Notably, 33 within avian host families there was no significant relationship between either host taxonomy or 34 foraging ecology and virome composition, although Anseriform species positive for influenza A 35 virus harboured more additional viruses than those negative for influenza virus. Overall, we 36 demonstrate complex virome structures across host species that co-exist in multi-species 37 aggregations. 38 39 Keywords: virus, evolution, host - pathogen interactions, influenza A virus, virome, wild birds 40 41 2 bioRxiv preprint doi: https://doi.org/10.1101/528174; this version posted January 29, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 42 Introduction 43 Many hosts are members of multi-species aggregations and may be infected by an assemblage of 44 specialist and/or multi-host generalist infectious agents. Host community diversity is central to 45 pathogen dynamics (1, 2), and pathogen species richness, relative abundance, specificity and intra- 46 and inter-species interactions within assemblages likely have complex roles in modulating pathogen 47 levels within populations (1, 3-8). A significant limitation in studying viral communities in hosts is 48 that most viral species remained undescribed (9), such that viral ecology across multi-host systems 49 has been limited to “single-virus” dynamics, particularly in vertebrate systems (for example, 50 Influenza A virus [IAV] in avian populations). With the advent of unbiased, bulk 'meta- 51 transcriptomic’ RNA sequencing we can now explore, in more detail, how viral community structure 52 may be shaped by host-species interactions. 53 Birds of the orders Anseriformes and Charadriiformes, the central reservoirs for avian viruses such 54 as IAV, avian avulavirus and avian coronavirus (10, 11), form multi-host flocks, in which many 55 species may migrate, forage, or roost together (e.g. (12). These flocks may comprise species along a 56 taxonomically related gradient and may utilize similar or different ecological niches in the same 57 environment. For example, in Australia, taxonomically related dabbling Grey Teals (Anas gracilis) 58 and Pacific Black Ducks (Anas superciliosa) may share the environment with the distantly related 59 filter feeding Pink-eared Duck (Malacorhynchus membranaceus). These multi-host flocks form 60 multi-host maintenance communities (6), with consequences for virus ecology, transmission, and 61 virulence (1, 13, 14). 62 Studies of the ecology of IAV, the best studied multi-host virus in wild birds, have shown that not all 63 hosts are equal (15, 16). In particular, there are marked differences in susceptibility, pathology and 64 the subsequent immune response in taxonomically related species, or distantly related species within 65 similar ecological niches. For example, dramatic differences in viral prevalence exist within the 66 Charadriiformes, such that Ruddy Turnstones (Arenaria interpres) may have an IAV prevalence of 67 ~15%, compared to the negligible IAV prevalence in co-sampled Sanderlings (Calidris alba) 68 sampled at Delaware Bay, USA (17). There are also major differences in the pathology of highly 69 pathogenic IAV in Anseriformes both in the field and in experimental infections. Mallards (Anas 70 platyrhynchos) infected with the highly pathogenic IAV are thought to move the virus large distances 71 and remain free of clinical signs, while Tufted Ducks (Aythya fuligula), in contrast, experience 72 severe mortality (18-20). Following IAV infection, dabbling ducks of the genus Anas are believed to 73 develop poor immune memory (21), allowing IAV re-infections throughout their lives, in contrast to 3 bioRxiv preprint doi: https://doi.org/10.1101/528174; this version posted January 29, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 74 swans that have long term immune memory (22) and where re-infection probability is likely very 75 low in adults. These differences are driven by factors encompassing both virus (e.g. virulence, 76 transmission) and host (e.g. receptor availability, immune responses) biology (11). 77 The goal of this study was to use the analysis of comparative virome structures, particularly virome 78 composition, diversity and abundance, as a means to describe the nature of host-virus interactions 79 beyond the “one-host, one-virus” model. Given their role as hosts for multi-host viruses such as IAV, 80 coronaviruses and avian avulaviruses, we used apparently healthy members of the Anseriformes and 81 Charadriiformes as model avian taxa in these comparisons. In particular, we aimed to (i) reveal the 82 viromes and describe novel viruses in the bird taxa sampled, (ii) determine whether viromes of 83 different host orders have different abundance and viral diversity such that they cluster separately, 84 (iii) determine whether closely taxonomically related and co-occuring avian hosts have viromes that 85 are more homogenous, and (iv) identify the impact of host taxonomy, which we use as a proxy for 86 differences in relevant host traits (such as host physiology, cell receptors), in determining virome 87 structure. Overall, we reveal a combination of virome heterogeneity and connectivity across avian 88 species that are important reservoirs of avian viruses. 89 90 Methods 91 Ethics statement 92 This research was conducted under approval of the Deakin University Animal Ethics Committee 93 (permit numbers A113-2010 and B37-2013). Banding was performed under Australian Bird Banding 94 Scheme permit (banding authority numbers 2915 and 2703). Research permits were approved by the 95 Department of Environment, Land, Water and Planning Victoria (permit numbers 10006663 and 96 10005726) 97 Sample selection 98 Samples were collected as part of a long-term IAV surveillance study (23, 24). Shorebirds were 99 captured using cannon nets at the Western Treatment Plant near Melbourne (37°59′11.62′′S, 113 100 144°39′38.66′′E) during the same sampling event (n=434). Waterfowl were sampled post-mortem 101 (within 12 hours) following harvest from lakes in south-west Victoria in March 2017 (n=125) 102 (36°58’S 141°05'E) (Table S1). No birds showed any signs of disease. 4 bioRxiv preprint doi: https://doi.org/10.1101/528174; this version posted January 29, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 103 A combination or oropharyngeal and cloacal samples were collected using a sterile-tipped swab and 104 were placed in viral transport media (VTM, Brain-heart infusion broth containing 2x106 122 U/l 105 penicillin, 0.2 mg/ml streptomycin, 0.5 mg/ml gentamicin, 500 U/ml amphotericin B, Sigma). 106 RNA virus discovery 107 RNA was extracted and libraries constructed as per (25) (Table S1). Paired end sequencing (100bp) 108 of the RNA library was performed on an Illumina platform at the Australian Genome Research 109 Facility (AGRF, Melbourne). Similarly, sequence reads were demultiplexed and contigs assembled 110 and contig abundance calculated as per (25).
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