Network analysis of the papaya orchard virome from two agroecological regions of Chiapas, Mexico

The study of complex ecological interactions - such as those among host, pathogen, and vector communities - can help to explain host ranges and the emergence of novel pathogens. The analysis of community structures using bipartite networks describe the associations between two trophic levels, for example plants and pollinators, or hosts and parasitoids. Bipartite networks represent interactions (links) occurring only between nodes in different levels - in our case, between viruses and hosts. We evaluated the viromes of papaya orchards (papaya, weeds, and insects) from intensive production of papaya in the Pacific Coastal Plain and the Central Depression of Chiapas, Mexico. Samples of papaya cultivar Maradol, which, like most cultivars, is susceptible to papaya ringspot virus (PRSV), were categorized by symptoms by local farmers (papaya ringspot symptoms, non-PRSV symptoms, or no symptoms). These analyses revealed the presence of 61 viruses, where only four species were shared among both physiographic regions. Nearly 52 complete viral genome sequences were recovered, of which 16 showed homology to known viruses, and 36 shared similarities with different genera including Potyvirus, Comovirus, and Tombusvirus (RNA viruses), and Begomovirus and Mastrevirus (DNA viruses). We analyzed the network of associations between viruses and host-location combinations, and described ecological properties of the network, such as asymmetry in interactions and nestedness compared to null models. Understanding the network structure informs management strategies, and advances understanding of interactions of hosts and viruses in the agroecological landscape.\n\nImportanceVirus-virus interactions in plants can modify host symptoms. As a result, disease management strategies may be unsuccessful if they are based solely on visual assessment and diagnostic assays for known individual viruses. Papaya ringspot virus is an important limiting factor for papaya production, and likely has interactions with other viruses that are not yet known. Using high-throughput sequencing, we recovered known and novel RNA and DNA viruses from papaya orchards in Chiapas, Mexico, categorized by host and, in the case of papaya, symptom type: asymptomatic papaya, papaya with ringspot virus symptoms, papaya with non-ringspot symptoms, weeds, and insects. Using network analysis, we demonstrated virus associations within and among host types, and described the ecological community patterns. Recovery of viruses from weeds and asymptomatic papaya suggests the need for additional management attention. These analyses contribute to the understanding of the community structure of viruses in the agroecological landscape.