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      Progress Out of a Pandemic: Global collections, data sharing, and changing standards of practice

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          Abstract

          The COVID-19 pandemic has disrupted all aspects of our lives, but has also spawned new opportunities. Months of multidisciplinary, global collaboration have explored the connections between natural history collections and COVID-19. Museums have unrivalled (and still largely untapped) potential to contribute data, methods, and expertise to prediction, mitigation, and prevention efforts related to zoonotic disease outbreaks (DiEuliis et al. 2016, Dunnum et al. 2017), and there is a clear need for ongoing collaboration across (at least) microbiology, disease ecology, and natural history collections. In addition, we note that the roadblocks to effective data access and integration related to microbes and their hosts are a microcosm of the larger data landscape; solving these issues in the context of COVID-19—from liberating data from publications to ensuring digital connections between voucher specimens and all derived viral genetic sequences—will improve biodiversity data access and use more broadly.Efforts since March 2020 have promoted collaboration across disciplines, international boundaries, and continents. At iDigBio, staff updated information about genetic/genomic resources available in US mammal collections; 24 records were added and information enhanced (Cortez and Soltis 2020). The Distributed System of Scientific Collections (DiSSCo) and the Consortium of European Taxonomic Facilities (CETAF) formed a worldwide COVID-19 Task Force (TaF). A US-led group formed the ViralMuse Task Force, working in concert with the TaF.Activities of the TaF centered on four areas: building a hub to coalesce knowledge from this group in a central location – including mining mammals-of-the-world literature, improving the metadata shared when publishing sequence data, encouraging virologists to voucher in museum collections, and gathering critical research questions around zoonotic disease from the scientific community. Through an online public event, this TaF shared work to date and critical next steps. Ongoing efforts include further refinement of metadata requirements for deposition of viral genetic data to include host specimen voucher identifiers, development of methods for better integration of bat and pathogen data from the literature and databases, analysis of community surveys, and development of webinars, symposia, and publications to report the work of the TaF. Members of the ViralMuse group worked to raise awareness of the critical value of and need for museum experts, collections data, and samples in any analyses of zoonotic events. ViralMuse members (Cook et al. 2020) stressed the need for collaborative action to:develop guidelines for keeping samples of both pathogens and hosts.  develop and implement metadata requirements for physical specimens and samples.expand investment in infrastructure, both cyber and physical, to support archives of biological materials. increase communication and development of new channels of dialogue and collaboration among museum scientists, microbiologists, bioinformaticians, biomedical professionals, and disease ecologists. enhance financial support and realize strong leadership from federal agencies, international partners, and private foundations to develop proactive, multi-disciplinary approaches to future pandemics (see also da Silva et al. 2020).ViralMuse continues to advance these goals. To reach a broader audience, we published an article in The Conversation (Soltis et al. 2020). A new project, funded by the US National Science Foundation (NSF), is aimed at enhancing existing published museum specimen data relevant to one potential reservoir of SARS-CoV-2, horseshoe bats (Mast and Paul 2020). NSF has also provided support to foster continued collaboration, infrastructure development, and integration of communities of practice concerning zoonotic diseases (Soltis and Paul 2020).From a TDWG perspective, issues relating to data access, data standards, and data integration require attention. Methods to liberate data from publications need to be expanded, and proposed metadata requirements for viral genetic sequences need to be implemented by international databases and adopted by the community. A summit on collections management software could help align efforts to both store and share the necessary host-pathogen information in standards-compliant formats that support discovery, access, and citation/attribution. A new and effective communication strategy is needed to develop an integrated research community (comprising the biodiversity, collections, data science, disease ecology, microbiology, and One Health communities) and to support needed changes in standards of practice (emphasizing vouchering, data standards, and data integration).

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          Biospecimen Repositories and Integrated Databases as Critical Infrastructure for Pathogen Discovery and Pathobiology Research

          Introduction A series of emerging pathogen outbreaks during the past 24 months (e.g., Ebola virus disease, Middle East respiratory syndrome, and Zika virus-associated microcephaly, and Guillain-Barre syndrome) have commanded the public’s attention and have exposed gaps in our preparedness to rapidly respond to these challenges. For example, the disease prevention and vector control response to the introduction and local spread of Zika virus infection in the United States is being blunted and hampered by congressional discord. Also, relying on legislation for emergency funds for each outbreak (rather than having a dedicated budget for preparedness and response to infectious disease outbreaks) is problematic. That said, previous zoonotic pathogen crises provide valuable insights into best practices, and herein, we detail the role of museum biorepositories in disease outbreak investigations. In addition to providing wide taxonomic sampling, museums and associated databases critically tie discoveries of new pathogens to permanent host records and samples and to a series of other informatics resources (e.g., GenBank and GIS applications) that facilitate future exploration, tracking, and mitigation of novel zoonotic pathogens. Because a fundamental requirement for the designation of a new pathogen is precise identification of the reservoir taxon [1], we advocate formal incorporation of museum biorepositories and integrated databases as critical infrastructure for pathogen discovery and pathobiology research. Case Study Approximately 40 years have passed since the identification of the striped field mouse (Apodemus agrarius) as the reservoir host of Haantan virus, the prototype virus of the genus Hantavirus in the family Bunyaviridae [2]. However, significant gains in our understanding of these pathogens did not occur until 1993, when an outbreak of a rapidly progressive, frequently fatal respiratory disease, now known as hantavirus pulmonary syndrome, was caused by Sin Nombre virus, a hantavirus harbored by the deer mouse (Peromyscus maniculatus) in the southwestern US [3]. That outbreak marked the beginning of integrated collaborations between public health agencies, virologists, ecologists, and museum scientists that completely reshaped our understanding of hantavirus systematics, evolution, and ecology. This interdisciplinary approach serves as a new model for pathogen discovery (Fig 1) and will be critical going forward as zoonotic pathogens and diseases emerge in the future [4]. Frozen tissues held in natural history museums stimulated discovery of many new hantaviruses in rodents (and, more recently, in shrews, moles, and bats) worldwide [5–6]. 10.1371/journal.pntd.0005133.g001 Fig 1 A museum-biorepository–based model for pathogen discovery and pathobiology research. Biorepositories and Databases Biomedical and pathobiology communities increasingly rely on archived human specimens to retroactively explore questions related to the etiology and pathogenesis of human diseases. Similarly, availability of frozen archives of wild vertebrates in museums permits rapid and efficient screening for diverse zoonotic pathogens and represents a major step forward in assessment, prevention, and mitigation of emerging diseases. Museum biorepositories have rigorous archival and database standards that ensure best practices are followed in pathogen discovery [7]. When new pathogens are described, permanent designation and deposition of host symbiotypes [8] provides a permanent link between samples and data (Fig 2). Macroparasites and microparasites present additional complexity due to their intimate association with particular host taxa. Host–parasite relationships critically require formal recognition to ensure not only that the original sample persists into the future but also that the identity of the pathogen reservoir will not be lost during the dynamic process of taxonomic revision. 10.1371/journal.pntd.0005133.g002 Fig 2 Pathogen symbiotype. Geo-referenced and time-stamped host specimen deposited in an accredited museum and linked through a single museum catalog number to ecological data, associated parasites, microbial pathogens, frozen tissues, genomic data, and publications derived from these materials. Recent analyses have revised the taxonomy of many zoonotic pathogen reservoirs, work that was only possible because the original host vouchers were preserved and available in museums. Many other species that serve as pathogen reservoirs are in need of critical taxonomic revision. For viruses, identification of reservoir species is often problematic (e.g., Ebola virus). Therefore, in-depth knowledge of potential hosts, their taxonomic affinities and relationships, and geographic distributions is vital [9]. We recommend several standardized procedures for integrating museum biorepository infrastructure into pathogen research (Table 1). 10.1371/journal.pntd.0005133.t001 Table 1 Recommendations. 1. Symbiotype designation: A single host specimen from which the novel pathogen was sequenced and/or isolated, and then described, should be formally designated. Taxonomy, museum catalog number (e.g., MSB:Mamm:89863), geo-referenced collection locality, date of collection, and institution of deposition should be included in the original publication. 2. Symbiotype deposition: Specimen, tissues, RNA and DNA extracts, and other ancillary material and data should be deposited and catalogued in an accredited natural history museum where all material will be permanently archived and available for future use by qualified investigators. 3. Pathogen name: Symbiotype catalog number should be included in the pathogen name (e.g., Camp Ripley virus [RPLV] MSB89863) to facilitate linkage. 4. GenBank accessions: Symbiotype identity should be confirmed with a DNA sequence (e.g., cytochrome b for mammals) deposited in GenBank. Both symbiotype and pathogen accession records should report the catalog number (e.g., MSB:Mamm:89863) in the “Definition” and “Specimen Voucher” data fields. 5. Database: The archiving institution should maintain a relational, web-accessible database (e.g., Arctosdb.org) linked to major biodiversity information servers (i.e., VertNet, GBIF, iDigBio) and directly to GenBank. 6. Archiving institution: Symbiotypes should be identified and managed as type specimens in the museum biorepository. Color-coded labels and notation in databases should identify the specimen as such. Traditional voucher material should be stored in a type case, and tissues should be held in a type rack in liquid nitrogen or -80°C freezers. 7. Symbiotype/pathogen list: List of symbiotypes and described pathogens held in a collection should be published or made available online. 8. Specimens examined and serology results: Should be included in publication or available as supplementary material. Although the fundamental utility of host voucher specimens and frozen tissue collections is recognized and has been championed by a few disease ecologists [10], wide acceptance of the concept is still lacking. Science advances as hypotheses are tested, experiments are replicated, and accumulated knowledge is reinterpreted in light of new information, tools, and analyses. Future availability of samples that produced the original, primary data is critical should questions arise regarding their nature, provenance, or taxonomic identity [11]. Over time, a single archived specimen (and associated GenBank sequence) may integrate across dozens of projects and subsequent publications [12], but because most GenBank accessions are not linked to specimens, we are too often unable to replicate or confirm data. With more than 20% of GenBank data potentially misidentified [13], the gold standard for GenBank accessions is now based on the voucher specimen concept [14]. We further advocate that all zoonotic pathogen descriptions provide molecular identification (nucleic acid sequence) for both the host and pathogen so that their identities can readily be placed on the Tree of Life [15] and provide a basis for identifying sister species that may serve as potential hosts for related pathogens. Future Directions Field collections of natural history specimens often arise through dynamic collaborations that are capable of producing a diverse array of preparations and associated data (e.g., ultra-frozen tissue, cell suspensions, feces, and endo- and ecto-parasites) with precise spatial and temporal stamps that facilitate myriad investigations. When properly archived and digitally captured, museum databases are capable of linking diverse kinds of “big data.” This biorepository nexus can be a powerful tool for research in pathogen discovery, environmental change, and host–reservoir dynamics. Spatially broad and temporally deep archives of ultra-frozen tissues represent unparalleled infrastructure for virologists, as demonstrated through the retrospective surveys for Sin Nombre hantavirus [16] and subsequent significant new hantavirus discoveries across four continents [5–6]. As tools for extracting vast amounts of information from both contemporary and ancient specimens improve [17], new insights into pathogen evolution and ecology will be enhanced [18]. We suggest that the benefits of incorporating this model into pathogen discovery and pathobiology research far outweigh any potential costs associated with its implementation (Box 1). Box 1. Advantages and Disadvantages of Museum Biorepositories and Integrated Databases Advantages: Maintains spatially broad, temporally deep and site-intensive archives of ultra-frozen vertebrate tissues Permanently links host specimens and tissues, microbial and host genetic sequences, associated publications, and other related data or materials Ensures that pathogen reservoir identity is not lost due to taxonomic revision Establishes best practices for loan agreements and specimen tracking Facilitates inclusion of museum catalog numbers in GenBank accessions prior to accepting manuscripts for publication Disadvantages: Necessitates long-term institutional commitment to support personnel and physical infrastructure Requires periodic inventory of the number and condition of biospecimens
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            Integrating Biodiversity Infrastructure into Pathogen Discovery and Mitigation of Emerging Infectious Diseases

            The global human suffering, economic damage, and social disruption we are currently experiencing from the COVID-19 pandemic stem from inadequate preparedness and ineffective response to emerging pathogens. At its core, the COVID-19 pandemic is a consequence of our fundamental ignorance of our planet's natural ecosystems and the effects of our encroachment on them. Our reactive approaches to the emergence of zoonotic pathogens, which are responsible for approximately 75% of all new emerging infectious disease outbreaks, are too often based on limited knowledge of the origin, pathogenicity, and basic biology of the wild host and pathogen coupled with poor communication among relevant stakeholders. Others have pointed to this ignorance of viral diversity and offered solutions (Andersen et al. 2020), but a broad, fully integrative discussion of how to leverage existing infrastructure and to build new resources has been missing. In the present article, we call for the development of alternative tactics that are aimed at proactively meeting the daunting challenges to humanity posed by emerging zoonotic pathogens. The potential role of natural history specimens in pathogen discovery and mitigation is recognized in the museum world (DiEuliis et al. 2016, Dunnum et al. 2017) and by at least some disease ecologists (e.g., Mills and Childs 1998). However, relatively few in the One Health community (e.g., Kelly et al. 2020) embrace the value of leveraging existing biodiversity infrastructure (i.e., natural history collections, biorepositories, and their associated expertise and informatics resources) to more fully understand zoonotic pathogen emergence and reemergence. This concept is not new; in the early 1900 s, the American Museum of Natural History created the Department of Public Health (Brown 2014). Although a lack of funding put an early end to the initiative, the Department of Public Health made extensive progress, from clever exhibitions for the public to assembling a living collection of bacterial cultures (Brown 2014). Renewed efforts to align pathobiology with biodiversity discovery initiatives are critical. Moreover, linking both biodiversity infrastructure and building capacity closer to zoonotic pathogen surveys in biodiverse countries would substantially improve proactive responses to pandemics before they once again wreak havoc across the globe. Biodiversity science as a tool in biomedical research and response Earth's biodiversity is connected through a single evolutionary tree of life, and pathogens (whether viruses, bacteria, or eukaryotes) and their hosts represent millions of years of evolutionary interactions. Medical researchers have long used this knowledge to advance our understanding of how certain microbes cause disease in humans. For example, because fundamental aspects of malaria parasitism are extremely difficult to study in humans, New World monkeys—­particularly, owl monkeys in the genus Aotus—have been important models for studying strains of malaria to develop vaccines, some of which are now in clinical trials. Taxonomic research based on museum specimens (Hershkovitz 1983) demonstrated that geographically separated species of owl monkeys have varying tolerance to the parasite and that the failure to recognize these taxonomic differences can hamper research. We have only begun to understand how widespread and diverse coronaviruses are in nature, and important gaps in regional and phylogenetic coverage persist (Anthony et al. 2017). Understanding their functional interactions with host cells and developing the most effective strategies to combat pathogenic coronaviruses will require documenting genetic relationships of the virus and among the wild hosts (Andersen et al. 2020). Archiving these associations in accessible and curated specimen databases is crucial now and into the future (e.g., www.globalbioticinteractions.org). Building on a solid foundation of knowledge of evolutionary and ecological relationships of hosts and pathogens enables scientists to possibly predict the emergence of future zoonotic diseases and to respond to novel outbreaks more rapidly and efficiently (Brooks et al. 2019). The need to strengthen biodiversity infrastructure and increase discovery The detection and description of novel pathogens usually requires large numbers of host samples because of low prevalence (Plowright et al. 2019). The world's natural history collections contain more than 3 billion specimens. Although the vast majority of these specimens may not be suitable for pathogen discovery, specimens provide a powerful roadmap to the spatial and temporal distribution of global biodiversity. A growing trend in many museums (e.g., www.idigbio.org/content/dna-banks-and-genetic-resources-repositories-united-states, www.ggbn.org) is the establishment of cryopreserved biorepositories, including vertebrate samples that often preserve associated parasites. These collections represent multiple, diverse host samples archived broadly across space and time that could readily be probed for pathogens. More commonly, however, novel pathogen discovery involves field surveys of wild hosts. Unless a particular pathogen is targeted, survey strategies that focus on taxonomically diverse species across spatially broad distributions provide the best opportunities for detection. Typically, field surveys of terrestrial vertebrates are noninvasive (using swabs or fecal samples) and do not produce archived specimens, so they rarely contribute to the shared biodiversity infrastructure of the world's scientific community. By instead linking these field surveys to permanent natural history collections, future pathogen discovery would be connected more broadly to other avenues of biodiversity research and naturally promote integration and synergy across scientific disciplines. An additional benefit from closer ties between pathobiology and natural history collections involves the voucher concept. Biodiversity studies, when possible, should be backed by a permanent sample or voucher, which would facilitate replication and validation, extension, and integration across disciplines (Cook et al. 2016, Lendemer et al. 2020). To date, few of the published nonhuman betacoronavirus sequences are tied to a permanent sample that would allow implementation of these central tenets of the scientific method (but see Joffrin et al. 2020). A change in practice, through improved communication between biodiversity and biomedical scientists, would both enhance the quality of any data collected from the pathogen and add value by enabling future analyses of the genotype, phenotype, and interactions of the same pathogen source. In addition to serving as permanent archives and providing samples for research, natural history collections and their associated biorepositories provide expertise in taxonomy, identification, phylogenetics, niche modeling, evolutionary dynamics, and other knowledge critical to pathogen monitoring, mitigation, and control. In the past few decades, museums have become hubs of biodiversity informatics, serving as the critical nexus between biological samples and sample-derived data (e.g., genomics, geographic information, isotope chemistry, CT scans). The current pandemic reminds us that natural history specimens are important but underappreciated reservoirs for studying the hosts and distributions of animal and human pathogens (see Harmon et al. 2019) and that the data connected to these specimens increase our understanding not only of the host organism but of the pathogens as well. Enhanced support of both physical and cyberinfrastructure for biodiversity collections would yield an information system to enable prediction and mitigation of future outbreaks and pandemics. The most biodiverse places on the planet occur in developing countries, so there is a huge need to develop local and regional capacity and scientific expertise in biodiversity research and collections. International scientific partnerships aiming to increase research transfer and building local capacity will help to match resources and technology available in developed countries. Therefore, it will facilitate early detection and mitigation in front of an outbreak. Given the tremendous need to understand how human-mediated loss of biodiversity and transformation of natural ecosystems will affect human health, building human capacity and strengthening ties between research and clinical infrastructure in developing countries is imperative. Informatics as a tool for disseminating knowledge Natural history institutions have produced extensive digital data and continue to digitize information from their physical collections. Online scientific databases (e.g., iDigBio, GBIF, VertNet, Arctos, Atlas of Living Australia, SpeciesLink) serve as portals to natural history archives, offering researchers around the world access to data and metadata (including linked genetic, environmental, and other information) associated with vouchered specimens. Furthermore, the development of this cyber-enabled information system is crucial for understanding our natural world and the relationships between biodiversity and human health. Connecting natural history archives and pathobiology is not only necessary but easier to achieve today than ever before. For example, free, online access to global specimen data provides efficient opportunities for loans of physical specimens from museums to biomedical laboratories for analysis of pathogens. Surprisingly, the robust cyberinfrastructure supporting living stock collections—which make viral, bacterial, and other pathogen lines and samples available to the biomedical research community—is not connected to that of natural history collections. These communities are only vaguely aware of each other's resources, despite obvious benefits for both basic and clinical research. However, a clear, long-term pathway must be implemented so that pathobiologists are fully aware of the varied resources available in natural history collections and can use and contribute to these resources. A new vision for predicting and responding to pandemics The twenty-first century has already seen multiple major new disease ­outbreaks—from SARS and MERS to Ebola and Zika—culminating in the current COVID-19 pandemic. What have we learned from these events, and how do we harness that knowledge for prediction and response? Ongoing encroachment by humans into natural ecosystems will continue to promote contact with potential pathogens. Absent global cooperation to restrict further habitat degradation and eliminate illegal wildlife trade, we need new approaches to gather, share, and interpret data and knowledge for deployment in preventing, predicting, and responding to future pandemics. We suggest five key elements as a framework for research and future resilience. Best practices must be developed for sample preparation. Biodiversity scientists, collections managers, disease ecologists, and microbiologists must converge on common guidelines for sampling, preserving, and archiving samples of both pathogens and hosts to ensure reproducible science and future access to samples studied in a particular context. Vouchering of host materials and pathogen preparations will require expanded capabilities in natural history collections and biorepositories, and cooperation among communities will be needed to ensure space and adequate curation of materials. Metadata requirements must be developed to accompany the physical specimens and samples collected, analyzed, and archived. The essential elements will be the application of universally unique identifiers for all specimens and their derivative products—including tissues, pathogen preparations, genetic sequences, and beyond. Again, communication among communities, including museum personnel, biomedical researchers, and personnel at global genetic databases, will be crucial for identifying and adopting metadata that will enhance the value of biological materials. Infrastructure, both physical and cyber, is required to support both current and future biological materials, whether in natural history collections, living stock collections, or other biorepositories. Because our knowledge of potential emerging pathogens is so limited and because the pathogens themselves evolve and diversify, we recommend expanded collection of field samples of organisms that are likely reservoirs of zoonotic diseases and other associated possible hosts. The preparation of these materials following the first element above will require expanded capacity and implementation of new curation methods in many institutions. Likewise, further investment in cyberinfrastructure to link together all known data and knowledge related to specimens, genetics, environment, literature, and more would enhance responses to future disease outbreaks. Perhaps the most important but most difficult element is the adoption and implementation of practices that change how a community conducts its science. We endorse open science concepts and practice and advocate increased communication and the development of new channels of dialogue and collaboration. This is particularly relevant within the integrative approaches to health that have increasingly become adopted, because they draw from multiple contributing sciences and sectors (Lerner and Berg 2017). The implementation of these elements requires strong leadership and financial support from a range of federal agencies, international partners, and private foundations worldwide to provide infrastructure and enable development of proactive approaches to future pandemics. Because the assets and returns are substantial for science, policy, and human well-being alike, we recommend that both research funders and the providers of official development aid engage in this effort. Such investment, even on the scale needed to accomplish the goals outlined in the present article, would be inconsequential compared to the loss of life and the economic catastrophe brought by COVID-19. Many of the pieces of our emerging vision are already in place, but a more resilient and integrated initiative that leverages and builds existing biodiversity infrastructure is critically needed.
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              Opinion: Specimen collections should have a much bigger role in infectious disease research and response

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                Author and article information

                Contributors
                Journal
                Biodiversity Information Science and Standards
                BISS
                Pensoft Publishers
                2535-0897
                October 09 2020
                October 09 2020
                : 4
                Article
                10.3897/biss.4.59268
                82ef7a46-cbdb-418f-ba74-718f2a79a3e4
                © 2020

                http://creativecommons.org/licenses/by/4.0/

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