Mass mortality in freshwater mussels (Actinonaias pectorosa) in the Clinch River, USA, linked to a novel densovirus

Abstract

freshwater mussels (order Unionida) are among the world's most biodiverse but imperiled taxa. Recent unionid mass mortality events around the world threaten ecosystem services such as water filtration, nutrient cycling, habitat stabilization, and food web enhancement, but causes have remained elusive. to examine potential infectious causes of these declines, we studied mussels in clinch River, Virginia and tennessee, USA, where the endemic and once-predominant pheasantshell (Actinonaias pectorosa) has suffered precipitous declines since approximately 2016. Using metagenomics, we identified 17 novel viruses in Clinch River pheasantshells. However, only one virus, a novel densovirus (Parvoviridae; Densovirinae), was epidemiologically linked to morbidity. Clinch densovirus 1 was 11.2 times more likely to be found in cases (moribund mussels) than controls (apparently healthy mussels from the same or matched sites), and cases had 2.7 (log 10) times higher viral loads than controls. Densoviruses cause lethal epidemic disease in invertebrates, including shrimp, cockroaches, crickets, moths, crayfish, and sea stars. Viral infection warrants consideration as a factor in unionid mass mortality events either as a direct cause, an indirect consequence of physiological compromise, or a factor interacting with other biological and ecological stressors to precipitate mortality. Freshwater mussels (order Unionida) are important members of freshwater biomes, providing ecosystem services such as water filtration, nutrient cycling and deposition, physical habitat stabilization, and food web enhancement 1. Mussels filter-feed on bacteria, suspended algae, detritus, phytoplankton and zooplankton 2 , removing suspended particulate matter from the water column and from interstitial spaces within the substrate. During periods of low summer discharge in small rivers, mussel assemblages are capable of circulating water as it flows over them, leading to multiple cycles of filtration 3 that can strongly influence ecosystem processes, even at moderate mussel densities 4. Unionids are also gaining attention for their ability to filter out chemical contaminants and water-borne pathogens 5-7. Unfortunately, the order Unionida contains an exceptional number of imperiled taxa. Among North America's 298 recognized unionid species 8 , > 70% are considered endangered, threatened, or vulnerable 9 , with 23 species having gone extinct from the Southeastern United States alone. Historically, habitat destruction (e.g., river impoundments), pollution, sedimentation, over-harvest for commercial use (most notably, pearl harvest and manufacture of shirt buttons from shells ca. 1850-1950) 10 , and competition from invasive species (e.g. the Asian clam Corbicula fluminea, zebra mussel Dreissena polymorpha, and quagga mussel D. bugensis) 11 have greatly reduced or extirpated many native mussel fauna. These threats have been present since the early twentieth century, mirroring trends in human development and land use 12 .

Virome Variation during Sea Star Wasting Disease Progression in Pisaster ochraceus (Asteroidea, Echinodermata)

“…Densoviruses ( Piccovirales ; Parvoviridae , ssDNA) have been previously recovered from arthropods (reviewed in [ 55 , 56 ]), mollusks [ 57 , 58 ], a tunicate [ 59 ] and echinoderms [ 2 , 5 , 6 , 7 ]. Densoviruses are associated with mussel [ 58 ] and asteroid ([ 2 ] but see [ 6 ]) mass mortality. Contigs matching densoviral proteins and genomes recovered in this survey bore primarily structural ORFs and ORFs bearing the non-structural (NS; i.e., replication-associated protein) 1 regions, with fewer NS2 and NS3 regions ( Figure 6 ).…”

Surveillance of densoviruses and mesomycetozoans inhabiting grossly normal tissues of three Aotearoa New Zealand asteroid species

“…Phylogenetic analyses based on NS1 revealed that Coscinasterias muricata contig 16413 was most similar to densoviruses recovered from Asterias rubens in Scotland [ 32 ] ( Fig 3 ). Phylogenetic analyses based on structural genes of the remaining viral contigs ( Coscinasterias muricata contig 15838 and Patiriella regularis contig 3718) suggested that these were most similar to ambidensoviruses from molluscs [ 33 , 34 ], insects [ 35 ], a crustacean [ 36 ], and human spinal fluid [ 37 ]. Quantitative PCR (qPCR) of the densovirus-like Coscinasterias muricata contig 15838 yielded only 3 DNQ results; two in Coscinasterias muricata (of 3 total surveyed) from Ti Point; and one Stichaster australis from Piha.…”

Surveillance of densoviruses and mesomycetozoans inhabiting grossly normal tissues of three New Zealand asteroid species

“…3). Phylogenetic analyses based on structural genes of the remaining viral contigs ( Coscinasterias muricata contig 15838 and Patiriella regularis contig 3718) suggested that these were most similar to ambidensoviruses from molluscs [26, 27], insects [28], a crustacean [29], and human spinal fluid [30]. Quantitative PCR (qPCR) of the densovirus-like Coscinasterias muricata contig 15838 yielded only 3 DNQ results; two in Coscinasterias muricata (of 3 total surveyed) from Ti Point; and one Stichaster australis from Piha.…”