Scavengers as Prospective Sentinels of Viral Diversity: the Snowy Sheathbill Virome as a Potential Tool for Monitoring Virus Circulation, Lessons from Two Antarctic Expeditions

Abstract

Antarctica is a unique environment due to its extreme meteorological and geological conditions. In addition to this, its relative isolation from human influences has kept it undisturbed. This renders our limited understanding of its fauna and its associated microbial and viral communities a relevant knowledge gap to fill. This includes members of the order Charadriiformes such as snowy sheathbills. They are opportunistic predator/scavenger birds distributed on Antarctic and sub-Antarctic islands that are in frequent contact with other bird and mammal species. This makes them an interesting species for surveillance studies due to their high potential for the acquisition and transport of viruses. In this study, we performed whole-virome and targeted viral surveillance for coronaviruses, paramyxoviruses, and influenza viruses in snowy sheathbills from two locations, the Antarctic Peninsula and South Shetland. Our results suggest the potential role of this species as a sentinel for this region. We highlight the discovery of two human viruses, a member of the genus Sapovirus GII and a gammaherpesvirus, and a virus previously described in marine mammals. Here, we provide insight into a complex ecological picture. These data highlight the surveillance opportunities provided by Antarctic scavenger birds. IMPORTANCE This article describes whole-virome and targeted viral surveillance for coronaviruses, paramyxoviruses, and influenza viruses in snowy sheathbills from the Antarctic Peninsula and South Shetland. Our results suggest an important role of this species as a sentinel for this region. This species' RNA virome showcased a diversity of viruses likely tied to its interactions with assorted Antarctic fauna. We highlight the discovery of two viruses of likely human origin, one with an intestinal impact and another with oncogenic potential. Analysis of this data set detected a variety of viruses tied to various sources (from crustaceans to nonhuman mammals), depicting a complex viral landscape for this scavenger species.

Keywords: Antarctica; emerging viruses; snowy sheathbill; surveillance; zoonosis.

FIG 1

Phylogenetic tree including members of the gamma- and deltacoronavirus genera. Sequence comparison was performed using 78 sequences from the gamma- and deltacoronavirus genera; the coronavirus isolated in our study (shown in green) appears to be closely related to a deltacoronavirus sequenced in 2009 and clusters with a sample of a partially sequenced virus from a gentoo penguin (shown in red). Phylogenetic distances were calculated using the GTR method. A bootstrap analysis with 1,000 replicates was applied, and the numbers indicate bootstrap values. (A) Complete phylogenetic tree; (B) zoomed-in view of the Antarctic sequence clade (green).

FIG 2

Locations of sampling sites for snowy sheathbills in the Antarctic Peninsula’s Harmony Point, Nelson Island, and Duroch Islands. Shown are the positions of sampling sites at the Southern Hemisphere scale (a) and the Antarctic Peninsula scale (b), the location of Harmony Point on Nelson Island (c), and the location for Kopaitic Island/Isabel Riquelme Islet on the Duroch Islands (d). Samples from locations in panel c were collected in 2020, and samples from locations in panel d were collected in 2022.

FIG 3

Avian influenza virus (AIV) seroprevalence in snowy sheathbills. Shown are data from competitive nucleoprotein (NP) ELISAs of serum samples obtained from snowy sheathbills. Rhombus dots display Isabel Riquelme Islet samples, and circles display Kopaitic Island samples. Overall, there was a 14% AIV seroprevalence. Abs, antibodies.

FIG 4

Krona plot representing an overview of all viral sequences identified by massively parallel sequencing. Taxa with >0.009% representation among the analyzed reads are shown in this Krona chart. Their names are included along with their percentages of representation. The relative abundance of viral sequences is displayed as follows: inner circles represent higher taxonomic ranks, and more detailed taxonomic ranks (up to the species level) are presented in the outer circles. An interactive version of this chart is available on the Krona website (see the URL listed in Materials and Methods). Navigational controls are at the top left, and details of the selected node are at the top right. The chart is zoomed in to place the “Viruses” domain at the root.

FIG 5

The snowy sheathbill as a sentinel of Antarctic viral diversity. Here, we display how the snowy sheathbill’s opportunistic feeding behavior can influence its harbored viral diversity and its likely source.

FIG 6

Phylogenetic tree including members of the Sapovirus genus. Sequence comparison was performed using 141 sequences from the Sapovirus genus; the sequence found in snowy sheathbills is highlighted by a red star. Phylogenetic distances were calculated using the Kimura 2-parameter method. A bootstrap analysis with 1,000 replicates was applied, and numbers indicate bootstrap values. All GenBank accession numbers are included in Tables S1 and S2 in the supplemental material. (A) Complete phylogenetic tree; (B) zoomed-in view of the clade including the newly identified sapovirus sequence.