Metagenomic and community-level sequencing efforts have revealed an astonishing diversity of viruses associated with grossly normal marine invertebrates. The vast majority of detected viruses likely represent asymptomatic infections under typical conditions, but may generate pathology in hosts under changing environmental conditions. Recent work concluded that sea star wasting (SSW) was a sequela of suboxic conditions that set up within boundary layers that overlie respiratory tissues, possibly fueled be heterotrophic remineralization of phytoplankton- and macroalgal-derived dissolved organic matter. This condition was accompanied by the proliferation of viruses, which was hypothesized to be due to enhanced replication as a consequence of oxygen stress. Hence, there is significant need to understand cues which trigger the switch between non-pathogenic and pathogenic viral infection and subsequent impacts on host biology and ecology. Sea cucumbers (Holothuroidea; Echinodermata) are ecologically important constituents of marine benthic habitats. Recent reports of a wasting-like condition concomitant with SSW suggest that similar factors may be at play. At the same time, we recently discovered a representative of the insect-only Flaviviruses, a deeply branched clade of enveloped positive sense single-stranded RNA viruses that includes important mammalian pathogens, in wasting holothurians. This proposal will investigate the ecology of this newly-discovered group in Parastichopus californicus by addressing three hypotheses: H1) Aquatic insect-only Flaviviruses (aiFVs) do not cause gross pathology under typical conditions; H2) aiFVs proliferate and generate clinical and gross pathology under suboxic stress; and H3) Periodic increases in primary production and mean temperature excursions cause aiFV proliferation and subsequently exacerbate holothurian disease process. The proposed study will comprise a restricted survey of aiFV diversity via amplicon sequencing and their prevalence within and between populations, the development of an antibody-based approach for aiFV detection, and examination of aiFV behavior in concert with host transcription and veterinary pathology. The study will also examine the impacts of representative organic matter enrichment on aiFVs and their hosts, and follow seasonal progression of aiFV within populations through citizen science-driven efforts. Finally, we will examine the impacts of phytoplankton productivity on aiFV dynamics in Apostichopus californicus.

The proposed work will provide transformative and mechanistic knowledge on the role of environmental conditions in marine metazoan viral prevalence, replication and disease process. The proposed work does not represent a wide survey of correlative genomes/genes with environmental conditions, but rather will focus on key, specific questions about the interactions between host gene expression and transcription factors, viral replication, and biological oceanographic conditions. We will employ a time series survey to ground truth experimental manipulations of oxygen, temperature, organic matter and simulated phytoplankton bloom collapse, and thereby directly tie together experimental parameters, host and viral genomic elements, and field conditions. Since enveloped +ssRNA viruses are not frequently encountered during surveys of host-associated viruses, our focused suite of observations will also provide transformative information about this enigmatic group of viruses.

Publications from this project:

Solomon C, Hewson I (2022) “Putative Invertebrate, Plant, and Wastewater Derived ssRNA Viruses in Plankton of the Anthropogenically Impacted Anacostia River, District of Columbia, USA” DOI: https://doi.org/10.1264/jsme2.ME21070

Oulhen N, Byrne M, Duffin P, Gomez-Chiarri M, Hewson I, Hodin J, Konar B, Lipp EK, Miner BG, Newton AL, Schiebelhut LM, Smolowitz R, Wahltinez SJ, Wessel GM, Work TM, Zaki HA, Wares JP (2022) “A Review of Asteroid Biology in the Context of Sea Star Wasting: Possible Causes and Consequences” Biological Bulletin. https://doi.org/10.1086/719928

Hewson I, Ritchie IT, Evans JS, Altera A, Behringer D, Bowman E, Brandt M, Budd KA, Camacho RA, Cornwell TO, Countway PD, Croquer A, Delgado GA, DeRito C, Duermit-Moreau E, Francis-Floyd R, Gittens S, Henderson L, Hylkema A, Kellogg CA, Kiryu Y, Kitson-Walters KA, Kramer P, Lang JC, Lessios H, Liddy L, Marancik D, Nimrod S, Patterson JT,  Pistor M, Romero IC, Sellares-Blasco R, Sevier MLB, Sharp WC,  Souza M, Valdez-Trinidad A, van der Laan M, Vilanova-Cuevas B, Villalpando M, Von Hoene SD, Warham M, Wijers T, Williams SM,  Work TM, Yanong RP, Zambrano S,  Zimmermann A,  Breitbart M (2023) “A scuticociliate causes mass mortality of Diadema antillarum in the Caribbean Sea” Science Advances. 9: DOI: 10.1126/sciadv.adg3200

Vilanova-Cuevas BY, Reyes-Chavez B, Breitbart M, Hewson I (2023) “Design and validation of a PCR protocol to specifically detect the clade of Philaster sp. associated with Diadema antillarum scuticociliatosis” biorxiv https://doi.org/10.1101/2023.09.11.557215

Crandell JG, Altera AK, DeRito CM, Hebert K, Markis J, Lim EG, Philipp KH, Rede JE, Schwartz ME, Vilanova-Cuevas BY, Wang E, Hewson I (2023) “Dynamics of the Apostichopus californicus-associated Flavivirus under suboxic conditions and organic matter amendment“. Frontiers in Marine Science https://doi.org/10.3389/fmars.2023.1295276

Ritchie IT, Vilanova-Cuevas B, Altera A, Cornfield K, Evans C, Evans JS, Hopson-Fernandes M, Kellogg CA, Looker E, Taylor O, Hewson I, Breitbart M (2024) “Transglobal spread of an ecologically relevant sea urchin parasite“. ISME Journal. 18: wrae024

Breitbart M, Hewson I (2024) “Coral reef ecology: Expanding urchin disease threatens ecosystem balance” Current Biology 34: PR578-R580

Rede JE, Breitbart M, Lundquist C, Nagasaki K, Hewson I (2024) “Diverse RNA viruses discovered in multiple seagrass species” PLoS One 19: e0302314 https://doi.org/10.1371/journal.pone.0302314

Hewson I, Johnson MR, Reyes-Chavez B  (2024) “Lessons learned from the sea star wasting investigation” Annual Reviews in Marine Science 17: https://doi.org/10.1146/annurev-marine-040623-082617

Hewson I, Brandt M, Budd K, Breitbart M, DeRito C, Gittens Jr S, Henson MW, Hylkema A, Sevier MLB, Souza M, Vilanova-Cuevas B, Von Hoene S (2024) “Viral metagenomic investigation of two Caribbean echinoderms, Diadema antillarum (Echinoidea) and Holothuria floridana (Holothuria)” PeerJ e18321

Vilanova-Cuevas B, Philipp KH, Altera AK, Apprill A, Becker CC, Behringer DC, Brandt ME, Breitbart M, Budd KA, DeRito CM, Duermit-Moreau E, Evans JE, Hopson-Fernandes M, Fleischer JA, Gittens Jr S, Henson MW, Hylkema A, Kellogg CA, Maritan AJ, Meyer JL, Pratte ZA, Ritchie IT, Sevier MLB, Souza M, Stewart FJ, Van Der Wal S, VonHoene S, Hewson I (2025) “Detection of the Diadema antillarum scuticociliatosis Philaster clade on sympatric metazoa, plankton and abiotic surfaces and assessment for its potential reemergence” Marine Ecology Progress Series https://doi.org/10.3354/meps14763

Vilanova-Cuevas B, DeRito CM, Ritchie IT, Kellogg CA, Evans JS, Zimmerman A, Williams SM, Brandt M, Sevier M, Gittens Jr S, Budd KA, Warham M, Sharp WC, Delgado GA, Hylkema A, Kitson-Walters K, Quod J-P, Breitbart M, Hewson I (2025) “Investigating the influence of Diadematidae scuticociliatosis on host microbiome composition” mSystems

Hewson I, Evans TM (2025) “Great Science Lost to Couriers: A Discussion of Best Practices for Shipping Scientific Research Materials at the 2025 Aquatic Sciences Meeting“. Limnology and Oceanography Bulletin. https://doi.org/10.1002/lob.10710

Hewson I (2025) “When bacteria meet many arms: Autecological insights into Vibrio pectinicida FHCF-3 in echinoderms” biorxiv https://doi.org/10.1101/2025.08.15.670479

Hein SA, Hewson I (2026) “Mass mortality of Diadema savignyi in Mo’orea in 2013” Marine Ecology Progress Series 782:meps15100

Hewson I, Rede JR (2026) “Investigating Marine Mass Mortality Using Rapid Nucleic Acid Sequencing and Artificial Intelligence: Going Back to Basics” in: Byers JE, Blakeslee AHM, Wares JP. The Ecology and Evolution of Marine Parasites and Disease. Oxford University Press