RNA virus diversity highlights the potential biosecurity threat posed by Antarctic krill

Tingting Xu , Xianyong Zhao , Thomas Loch , Jiancheng Zhu , Wei Wang , Xinliang Wang , Chong Wang , Gangzhou Fan , Bin Hao , Jichang Zhang , Wenxiu Zhao , Melba G. Bondad-Reantaso , Victoria Alday-Sanz , Qingli Zhang

Marine Life Science & Technology ›› 2025, Vol. 7 ›› Issue (1) : 96 -109.

PDF
Marine Life Science & Technology ›› 2025, Vol. 7 ›› Issue (1) :96 -109. DOI: 10.1007/s42995-024-00270-w
Research Paper
research-article
RNA virus diversity highlights the potential biosecurity threat posed by Antarctic krill
Author information +
History +
PDF

Abstract

Antarctic krill Euphausia superba, one of the most abundant species on the planet, is a keystone species of the Southern Ocean ecosystem. In the present study, we analyzed the RNA virome of Antarctic krill via metatranscription methods. The results showed that only 0.39% (49/12, 558) of the resultant unigenes could be assigned to known viral taxa, which were most similar to 17 known viruses, including nine invertebrate viruses, two vertebrate viruses, three protozoan viruses and three mycoviruses. However, most of the detected viruses possessed low amino acid similarity with counterparts in the viral databases. Penaeus vannamei picornavirus (PvPV; Family Picornaviridae) and covert mortality nodavirus (CMNV; Family Nodaviridae) were the two most abundant viruses in the Antarctic krill RNA virome. Notably, PvPV and CMNV are known pathogens to multiple aquatic animals according to epidemiological survey and exposure experiments, whereby PvPV positive krill caused clinical symptoms and histopathological lesions to P. vannamei and similarly, CMNV infection altered the swimming and feeding behavior of parent marine medaka Oryzias melastigma and caused tissue damage and even spinal curvature of the offspring. Results herein reveal, for the first time, the high abundance and taxonomic diversity of viruses in Antarctic krill while simultaneously highlighting the risk of an important virus reservoir to global aquaculture, and the potential impact on animals in the Antarctic ecosystem.

Keywords

RNA virome / Antarctic krill Euphausia superba / Biosafety / Global aquaculture / Antarctic ecosystem

Cite this article

Download citation ▾
Tingting Xu, Xianyong Zhao, Thomas Loch, Jiancheng Zhu, Wei Wang, Xinliang Wang, Chong Wang, Gangzhou Fan, Bin Hao, Jichang Zhang, Wenxiu Zhao, Melba G. Bondad-Reantaso, Victoria Alday-Sanz, Qingli Zhang. RNA virus diversity highlights the potential biosecurity threat posed by Antarctic krill. Marine Life Science & Technology, 2025, 7(1): 96-109 DOI:10.1007/s42995-024-00270-w

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Akiyama T, Murai T, Hirasawa Y, Nose T. Supplementation of various meals to fish meal diet for chum salmon fry. Aquaculture. 1984, 37: 217-222

[2]

Allahpichay I, Shimizu C. Extraction of growth promoting fractions from non-muscle krill meal of Euphausia superba and its effect on fish growth. Bull Jpn Soc Sci Fish. 1984, 50: 821-826

[3]

Brum JR, Ignacio-Espinoza JC, Roux S, Doulcier G, Acinas SG, Alberti A, Chaffron S, Cruaud C, De Vargas C, Gasol JM. Patterns and ecological drivers of ocean viral communities. Science. 2015, 348: 1261-1498

[4]

Cao S, Zhang W, Ding W, Chen XL. Structure and function of the Arctic and Antarctic marine microbiota as revealed by metagenomics. Microbiome. 2020, 8: 47

[5]

Cavan EL, Belcher A, Atkinson A, Hill SL, Kawaguchi S, Mccormack S, Meyer B, Nicol S, Ratnarajah L, Schmidt K. The importance of Antarctic krill in biogeochemical cycles. Nat Commun. 2019, 10: 4742

[6]

Cavicchioli R, Erdmann S. The discovery of Antarctic RNA viruses: a new game changer. Mol Ecol. 2015, 24: 4809-4811

[7]

Chown SL, Convey P. Spatial and temporal variability across life’s hierarchies in the terrestrial Antarctic. Philos Trans R Soc Lond B Biol Sci. 2007, 1488: 2307-2331

[8]

Chown SL, Clarke A, Fraser CI, Cary SC, Moon KL, McGeoch MA. The changing form of Antarctic biodiversity. Nature. 2015, 522: 431-438

[9]

Convey P, Smith R. Geothermal bryophyte habitats in the South Sandwich Islands, maritime Antarctic. J Veg Sci. 2010, 17: 529-538

[10]

Daniel ADC, Alberto LB, Alonso-Lobo JM, Antonio Q, Antonio A (2016) Metagenomic analysis of lacustrine viral diversity along a latitudinal transect of the Antarctic Peninsula. FEMS Microbiol Ecol 92

[11]

Dietzgen RG, Bejerman NE, Goodin MM, Higgins CM, Huot OB, Kondo H, Martin KM, Whitfield AE. Diversity and epidemiology of plant rhabdoviruses. Virus Res. 2020, 281: 197942

[12]

El-Sayed A, Kamel M. Future threat from the past. Environ Sci Pollut Res Int. 2021, 28: 1287-1291

[13]

Fischer MG, Allen MJ, Wilson WH, Suttle CA. Giant virus with a remarkable complement of genes infects marine zooplankton. Pro Natl Acad Sci. 2010, 107: 19508-19513

[14]

Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng QD, Chen ZH, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, et al. . Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011, 29: 644-652

[15]

Gregory AC, Zayed AA, Conceição-Neto N, Temperton B, Bolduc B, Alberti A, Ardyna M, Arkhipova K, Carmichael M, Cruaud C, Dimier C, Domínguez-Huerta G, Ferland J, Kandels S, Liu YX, Marec C, Pesant S, Picheral M, Pisarev S, Poulain J, et al. . Marine DNA viral macro- and microdiversity from pole to pole. Cell. 2019, 177: 109-1123

[16]

Hause BM, Nelson E, Hennings JC. Novel and diverse non-Rabies Rhabdoviruses identified in bats with human exposure, South Dakota, USA. Viruses. 2020, 12: 1408

[17]

Ignacio-Espinoza JC, Ahlgren NA, Fuhrman JA. Long-term stability and Red Queen-like strain dynamics in marine viruses. Nat Microbiol. 2020, 5: 265-271

[18]

Lambrechts S, Willems A, Tahon G. Uncovering the uncultivated majority in Antarctic soils: toward a synergistic approach. Front Microbiol. 2019, 10: 242

[19]

Lee SY, Kim JH, Seo TK, No JS, Kim H, Kim WK, Choi HG, Kang SH, Song J W (2016) Genetic and molecular epidemiological characterization of a novel Adenovirus in Antarctic Penguins collected between 2008 and 2013. PloS ONE 11

[20]

Letko M, Seifert SN, Olival KJ, Plowright RK, Munster VJ. Bat-borne virus diversity, spillover and emergence. Nat Rev Microbiol. 2020, 18: 461-471

[21]

Li XP, Wan XY, Xu TT, Huang J, Zhang QL. Development and validation of a TaqMan RT-Qpcr for the detection of convert mortality nodavirus (CMNV). J Virol Methods. 2018, 262: 65-71

[22]

Li XP, Wan XY, Zhang QL, Huang J, Dong X, Wang XH, Qiu L, Song ZL, Cheng DY. Molecular epidemiological survey of covert mortality nodavirus (CMNV) in cultured crustaceans in China in 2016–2017. Prog Fish Sci. 2019, 40: 65-73In Chinese

[23]

Li XP, Wan XY, Zhang QL, Huang J, Dong X, Wang XH, Qiu L, Song ZL, Chen DY. Molecular epidemiological survey on covert mortality nodavirus (CMNV) in cultured crustacean in China in 2016–2017. Prog Fish Sci. 2019, 40: 65-73In Chinese

[24]

Lima-Mendez G, Faust K, Henry N, Decelle J, Colin S, Carcillo F, Chaffron S, Ignacio-Espinosa JC, Roux S, Vincent F, Bittner L, Darzi Y, Wang J, Audic S, Berline L, Bontempi G, Cabello AM, Coppola L, Cornejo-Castillo FM, d’Ovidio F, et al. . Determinants of community structure in the global plankton interactome. Science. 2015, 348: 1262-2037

[25]

Liu WZ, Fan YD, Li Z, Zhao JQ, Zhou Y, Zeng NJ, Zeng LB. Isolation, identification, and classification of a novel rhabdovirus from diseased Chinese rice-field eels (Monopterus albus). Arch Virol. 2019, 164: 105-116

[26]

Liu S, Xu TT, Wang C, Jia TC, Zhang QL. A novel picornavirus discovered in white leg shrimp Penaeus vannamei. Viruses. 2021, 13: 2381

[27]

Lloyd-Smith JO. Predictions of virus spillover across species. Nature. 2017, 546: 603-604

[28]

Lopez-Bueno A, Tamames J, Velazquez D, Moya A, Quesada A, Alcamí A. High diversity of the viral community from an Antarctic lake. Science. 2009, 326: 858-861

[29]

Mann NH, Cook A, Millard A, Bailey S, Clokie M. Marine ecosystems: bacterial photosynthesis genes in a virus. Nature. 2003, 424: 741

[30]

Meyer B, Atkinson A, Bernard KS, Brierley AS, Driscoll R, Hill SL, Marschoff E, Maschette D, Perry FA, Reiss CS, Rombolá E, Tarling GA, Thorpe SE, Trathan PN, Zhu GP, Kawaguchi S. Successful ecosystem-based management of Antarctic krill should address uncertainties in krill recruitment, behaviour and ecological adaptation. Commun Earth Environ. 2020, 1: 28

[31]

Miner KR, D’Andrilli J, Mackelprang R, Edwards A, Malaska MJ, Waldrop MP, Miller CE. Emergent biogeochemical risks from Arctic permafrost degradation. Nat Clim Change. 2021, 11: 809-819

[32]

Ou T, Zhu RL, Chen ZY, Zhang QY. Isolation and identification of a lethal rhabdovirus from farmed rice field eels Monopterus albus. Dis Aquat Org. 2013, 106: 197-206

[33]

Plowright RK, Eby P, Hudson PJ, Smith IL, Westcott D, Bryden WL, Middleton D, Reid PA, McFarlane RA, Martin G, Tabor GM, Skerratt LF, Anderson DL, Crameri G, Quammen D, Jordan D, Freeman P, Wang LF, Epstein JH, Marsh GA, et al. . Ecological dynamics of emerging bat virus spillover. P R Soc B-Biol Sci. 2015, 282: 20142124

[34]

Pooljun C, Direkbusarakom S, Chotipuntu P, Hirono I, Wuthisuthimethavee S. Development of a TaqMan real-time RT-PCR assay for detection of covert mortality nodavirus (CMNV) in penaeid shrimp. Aquaculture. 2016, 464: 445-450

[35]

Pruitt KD, Tatusova T, Maglott DR. vNCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 2007, 35: D61-D65

[36]

Quetin LB, Ross RM, Fritsen CH, Vernet M. Ecological responses of Antarctic krill to environmental variability: Can we predict the future?. Antarct Sci. 2007, 19: 253-266

[37]

Rodriguez-Valera F, Martin-Cuadrado AB, Rodriguez-Brito B, Pašić L, Thingstad TF, Rohwer F, Mira A. Explaining microbial population genomics through phage predation. Nat Rev Microbiol. 2009, 7: 828-836

[38]

Roux S, Brum JR, Dutilh BE, Sunagawa S, Duhaime MB, Loy A, Poulos BT, Solonenko N, Lara E, Poulain J, Pesant S, Kandels-Lewis S, Dimier C, Picheral M, Searson S, Cruaud C, Alberti A, Duarte CM, Gasol JM, Vaqué D, et al. . Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature. 2016, 537: 689-693

[39]

Schulz F, Roux S, Paez-Espino D, Jungbluth S, Walsh DA, Denef VJ, McMahon KD, Konstantinidis KT, Eloe-Fadrosh EA, Kyrpides NC, Woyke T. Giant virus diversity and host interactions through global metagenomics. Nature. 2020, 578: 432-436

[40]

Shi M, Lin XD, Tian JH, Chen LJ, Chen X, Li CX, Qin XC, Li J, Cao JP, Eden JS, Buchmann J, Wang W, Xu JG, Holmes EC, Zhang YZ. Redefining the invertebrate RNA virosphere. Nature. 2016, 540: 539-543

[41]

Smeele ZE, Burns JM, Doorsaler KV, Fontenele RS, Waits K, Stainton D, Shero MR, Beltran RS, Kirkham AL, Berngartt R, Kraberger S, Varsani A. Diverse papillomaviruses identified in Weddell seals. J Gen Virol. 2018, 99: 549-557

[42]

Subasinghe R, Alday-Sanz V, Bondad-Reantaso MG, Jie H, Shinn AP, Sorgeloos P. Biosecurity: reducing the burden of disease. J World Aquacult Soc. 2023, 54: 397-426

[43]

Sun S, Liu YQ. Antarctic krill and the Southern Ocean ecosystem. Chin J Nat. 2009, 31: 88

[44]

Suttle CA. Viruses in the sea. Nature. 2005, 437: 356-361

[45]

Sylvester ZT, Long MC, Brooks CM. Detecting climate signals in Southern Ocean Krill growth habitat. Front Mar Sci. 2021, 8: 708

[46]

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011, 28: 2731-2739

[47]

Tao JJ, Gui JF, Zhang QY. Isolation and characterization of a rhabdovirus from co-infection of two viruses in mandarin fish. Aquaculture. 2007, 262: 1-9

[48]

Thitamadee S, Prachumwat A, Srisala J, Jaroenlak P, Salachan PV, Sritunyalucksana K, Flegel TW, Itsathitphaisarn O. Review of current disease threats for cultivated penaeid shrimp in Asia. Aquaculture. 2016, 452: 69-87

[49]

Thompson CC, Wasielesky W, Landuci F, Lima MS, Bacha L, Perazzolo L, Lourenço-Marques C, Soares F, Pousão-Ferreira P, Hanson L, Gomez-Gil B, Thompson M, Varasteh T, A. Silva T, Swings J, Zhang XH, Souza WD, Thompson FL (2024) Understanding the role of microbes in health and disease of farmed aquatic organisms. Mar Life Sci Technol 6:579–609

[50]

Van Etten JL. Another really, really big virus. Viruses. 2011, 3: 32-46

[51]

Varsani A, Frankfurter G, Stainton D, Male MF, Kraberger S, Burns JM. Identification of a polyomavirus in Weddell seal (Leptonychotes weddellii) from the Ross Sea (Antarctica). Arch Virol. 2017, 162: 1403-1407

[52]

Wang C, Liu S, Li XP, Hao JW, Zhang QL. Infection of covert mortality nodavirus in Japanese flounder reveals host jump of the emerging alphanodavirus. J Gen Virol. 2019, 100: 166-175

[53]

Wang C, Wang XH, Liu S, Sang SW, Zhang QL. Preliminary study on the natural infection of Carassius auratus with covert mortality nodavirus (CMNV). J Fish Sci China. 2019, 40: 25-32In Chinese

[54]

Wang C, Liu S, Tang KFJ, Zhang QL. Natural infection of covert mortality nodavirus affects Zebrafish (Danio rerio). J Fish Dis. 2021, 44: 1315-1324

[55]

Wang W, Liu S, Yao L, Xia JT, Xu TT, Wang C, Li C, Zhang QL. Development of a novel RT-qPCR detecting method of covert mortality Nodavirus (CMNV) for the national proficiency test in molecular detection. Viruses-Basel. 2022, 14: 1475

[56]

Welsh JE, Steenhuis P, de-Moraes KR, van der Meer J, Thieltges DW, Brussaard CPD. Marine virus predation by non-host organisms. Sci Rep. 2020, 10: 5221

[57]

Wille M, Harvey E, Shi M, Gonzalez-Acuña D, Holmes EC, Hurt AC. Sustained RNA virome diversity in Antarctic penguins and their ticks. ISME J. 2020, 14: 1768-1782

[58]

Wilson JM, Bunte RM, Carty AJ. Evaluation of rapid cooling and tricaine methanesulfonate (MS222) as methods of euthanasia in zebrafish (Danio rerio). J Am Assoc Lab Anim. 2009, 48: 785-789

[59]

Wu WP, Xie YL (2010) Antarctic Krill and Krill Fisheries. Modern Fish Inf 25 (In Chinese)

[60]

Xu TT, Li YX, Shan XJ, Hao JW, Teng GL, Tang KFJ, Zhang QL, Yao CL. Natural infection of covert mortality Nodavirus in small yellow croaker in coastal water. Front Mar Sci. 2021, 8: 670831

[61]

Yau S, Seth-Pasricha M. Viruses of polar aquatic environments. Viruses. 2019, 11: 189

[62]

Yoshitomi B, Nagano I. Effect of dietary fluoride derived from Antarctic krill (Euphausia superba) meal on growth of yellowtail (Seriola quinqueradiata). Chemosphere. 2012, 86: 891-897

[63]

Zachos J, Pagani M, Sloan L, Thomas E, Billups K. Trends, rhythms, and aberrations in global climate 65Ma to present. Science. 2001, 291: 1511-1517

[64]

Zeng W, Wang Q, Wang Y, Liu C, Liang H, Fang X, Wu S. Genomic characterization and taxonomic position of a rhabdovirus from a hybrid snakehead. Arch Virol. 2014, 159: 2469-2473

[65]

Zhang QL, Liu Q, Liu S, Yang HL, Liu S, Zhu LL, Yang B, Jin JT, Ding LX, Wang XH, Liang Y, Wang QT, Huang J. A new nodavirus is associated with covert mortality disease of shrimp. J Gen Virol. 2014, 95: 2700-2709

[66]

Zhang QL, Liu S, Yang HL, Zhu LL, Wan XY, Li XP, Huang J. Reverse transcription loop mediated isothermal amplification for rapid and quantitative assay of covert mortality nodavirus in shrimp. J Invertebr Pathol. 2017, 150: 130-135

[67]

Zhang QL, Liu S, Li J, Xu TT, Wang XH, Fu GM, Li XP, Sang SW, Bian XD, Hao JW. Evidence for cross-species transmission of covert mortality nodavirus to new host of Mugilogobius abei. Front Microbiol. 2018, 9: 1447

RIGHTS & PERMISSIONS

The Author(s)

PDF

2

Accesses

0

Citation

Detail

Sections
Recommended

/