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Volume 8, Issue 7

Comparative genomics of reveals recent importation and subsequent widespread dissemination in mariculture farms in the South Central Coast region, Vietnam Open Access

Abstract

Between 2010 and 2015, nocardiosis outbreaks caused by affected many permit farms throughout Vietnam, causing mass fish mortalities. To understand the biology, origin and epidemiology of these outbreaks, 20 . strains collected from farms in four provinces in the South Central Coast region of Vietnam, along with two Taiwanese strains, were analysed using genetics and genomics. PFGE identified a single cluster amongst all Vietnamese strains that was distinct from the Taiwanese strains. Like the PFGE findings, phylogenomic and SNP genotyping analyses revealed that all Vietnamese strains belonged to a single, unique clade. Strains fell into two subclades that differed by 103 SNPs, with almost no diversity within clades (0–5 SNPs). There was no association between geographical origin and subclade placement, suggesting frequent transmission between Vietnamese mariculture facilities during the outbreaks. The Vietnamese strains shared a common ancestor with strains from Japan and China, with the closest strain, UTF1 from Japan, differing by just 220 SNPs from the Vietnamese ancestral node. Draft Vietnamese genomes range from 7.55 to 7.96 Mbp in size, have an average G+C content of 68.2 % and encode 7 602–7958 predicted genes. Several putative virulence factors were identified, including genes associated with host cell adhesion, invasion, intracellular survival, antibiotic and toxic compound resistance, and haemolysin biosynthesis. Our findings provide important new insights into the epidemiology and pathogenicity of and will aid future vaccine development and disease management strategies, with the ultimate goal of nocardiosis-free aquaculture.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): aquaculture , fish infection , fish mortality , genomics , infectious disease , Nocardia seriolae , nocardiosis , permit fish and trachinotus
© 2022 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2022-07-04
2024-04-29
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References

  1. Berry F, Iversen ES. Pompano: biology, fisheries, and farming potential. Proc Annu Gulf Caribb Fish Inst 1967; 19:116–128
     [Google Scholar]
  2. Finucane JH. Ecology of the pompano (Trachinotus carolinus) and the permit (T. falcatus) in Florida. Trans Am Fish Soc 1969; 98:478–486 [View Article]
     [Google Scholar]
  3. Muller RG, Tisdel K, Murphy MD. The 2002 update of the stock assessment of Florida pompano (Trachinotus carolinus) St Petersburg, FL: Florida Fish and Wildlife Conservation Commission, Florida Marine Research Institute; 2002
     [Google Scholar]
  4. McMaster M, Kloth T, Coburn J. Prospects for commercial pompano mariculture. In Aquaculture America 2003 Exhibition and Conference (18th-21st Feb 2003, Louisville, KY, USA) 2003 https://mariculturetechnology.com/wp-content/uploads/2019/07/AquacultureAmerica03.pdf
     [Google Scholar]
  5. Tutman P, Glavić N, Kožul V, Skaramuca B, Glamuzina B. Preliminary information on feeding and growth of pompano, Trachinotus ovatus (Linnaeus, 1758) (Pisces; Carangidae) in captivity. Aquaculture International 2004; 12:387–393 [View Article]
     [Google Scholar]
  6. Klinkhardt M, Myrseth B. New aquaculture candidates. Global Trade Conference on Aquaculture 2007
     [Google Scholar]
  7. Juniyanto MN, Akbar S. Breeding and seed production of silver pompano (Trachinotus blochii, Lacepede) at the mariculture development center of batam. Providing Claims Services to the Aquaculture Industry 2008; 8:46–48
     [Google Scholar]
  8. FAO Global Aquaculture Production. online query 2021 http://www.fao.org/fishery/statistics/global-aquaculture-production/query/en accessed 10 June 2021
     [Google Scholar]
  9. Giang N, Binh D, Hoa D. Preliminary study of white spot disease in internal organs in snubnose pompano (Trachinotus blochii). J Fish Sci Technol 2012; 4:26–33
     [Google Scholar]
  10. Vu-Khac H, Duong VQ, Chen S-C, Pham TH, Nguyen TT et al. Isolation and genetic characterization of Nocardia seriolae from snubnose pompano Trachinotus blochii in Vietnam. Dis Aquat Organ 2016; 120:173–177 [View Article] [PubMed]
     [Google Scholar]
  11. Kariya T, Kubota S, Nakamura Y, Kira K. Nocardial infection in cultured yellowtails (Seriola quinqueruiata and S. purpurascens)—I. Fish Pathol 1968; 3:16–23 [View Article]
     [Google Scholar]
  12. Kusuda R, Salati F. Major bacterial diseases affecting mariculture in Japan. Annu Rev Fish Dis 1993; 3:69–85 [View Article]
     [Google Scholar]
  13. Kudo T, Hatai K, Seino A. Nocardia seriolae sp. nov. causing nocardiosis of cultured fish. Int J Syst Bacteriol 1988; 38:173–178 [View Article]
     [Google Scholar]
  14. Chen S, Tung M, Tsai W. An epizootic in Formosa snake-head fish, Channa maculata Lacepede, caused by Nocardia asteroides in fresh water pond in Southern Taiwan. COA Fisheries Series 1989; 15:42–48
     [Google Scholar]
  15. Chen S, Tung M. An epizootic in large mouth bass, Micropterus salmoides, lacepede caused by Nocardia asteroides in freshwater pond in Southern Taiwan. J Chin Soc Vet Sci 1991; 17:15–22 [View Article]
     [Google Scholar]
  16. Chen S-C, Lee J-L, Lai C-C, Gu Y-W, Wang C-T et al. Nocardiosis in sea bass, Lateolabrax japonicus, in Taiwan. J Fish Dis 2000; 23:299–307 [View Article]
     [Google Scholar]
  17. Huang S. Isolation and characterization of the pathogenic bacterium, Nocardia seriolae, from female broodstock of striped mullet (Mugil cephalus). J Fish Res 2004; 12:61–69
     [Google Scholar]
  18. Park M, Lee D-C, Cho M-Y, Choi H-J, Kim J-W. Mass mortality caused by nocardial infection in cultured snakehead, Channa arga in Korea. J Fish Pathol 2005; 18:157–165
     [Google Scholar]
  19. Shimahara Y, Nakamura A, Nomoto R, Itami T, Chen S-C et al. Genetic and phenotypic comparison of Nocardia seriolae isolated from fish in Japan. J Fish Dis 2008; 31:481–488 [View Article] [PubMed]
     [Google Scholar]
  20. Shimahara Y, Huang Y-F, Tsai M-A, Wang P-C, Yoshida T et al. Genotypic and phenotypic analysis of fish pathogen, Nocardia seriolae, isolated in Taiwan. Aquaculture 2009; 294:165–171 [View Article]
     [Google Scholar]
  21. Cornwell ER, Cinelli MJ, McIntosh DM, Blank GS, Wooster GA et al. Epizootic Nocardia infection in cultured weakfish, Cynoscion regalis (Bloch and Schneider). J Fish Dis 2011; 34:567–571 [View Article] [PubMed]
     [Google Scholar]
  22. Kim JD, Lee N-S, Do JW, Kim MS, Seo HG et al. Nocardia seriolae infection in the cultured eel Anguilla japonica in Korea. J Fish Dis 2018; 41:1745–1750 [View Article] [PubMed]
     [Google Scholar]
  23. Del Rio-Rodriguez RE, Ramirez-Paredes JG, Soto-Rodriguez SA, Shapira Y, Huchin-Cortes MDJ et al. First evidence of fish nocardiosis in Mexico caused by Nocardia seriolae in farmed red drum (Sciaenops ocellatus, Linnaeus). J Fish Dis 2021; 44:1117–1130 [View Article]
     [Google Scholar]
  24. Imajoh M, Fukumoto Y, Yamane J, Sukeda M, Shimizu M et al. Draft genome sequence of Nocardia seriolae Strain N-2927 (NBRC 110360), isolated as the causal agent of nocardiosis of yellowtail (Seriola quinqueradiata) in Kochi Prefecture, Japan. Genome Announc 2015; 3:e00082-15 [View Article]
     [Google Scholar]
  25. Xia L, Cai J, Wang B, Huang Y, Jian J et al. Draft genome sequence of Nocardia seriolae ZJ0503, a fish pathogen isolated from Trachinotus ovatus in China. Genome Announc 2015; 3:e01223–01214 [View Article] [PubMed]
     [Google Scholar]
  26. Imajoh M, Sukeda M, Shimizu M, Yamane J, Ohnishi K et al. Draft genome sequence of erythromycin- and oxytetracycline-sensitive Nocardia seriolae strain U-1 (NBRC 110359). Genome Announc 2016; 4:e01606–01615 [View Article] [PubMed]
     [Google Scholar]
  27. Yasuike M, Nishiki I, Iwasaki Y, Nakamura Y, Fujiwara A et al. Analysis of the complete genome sequence of Nocardia seriolae UTF1, the causative agent of fish nocardiosis: the first reference genome sequence of the fish pathogenic Nocardia species. PLoS One 2017; 12:e0173198 [View Article] [PubMed]
     [Google Scholar]
  28. Han H-J, Kwak M-J, Ha S-M, Yang S-J, Kim JD et al. Genomic characterization of Nocardia seriolae strains isolated from diseased fish. Microbiologyopen 2019; 8:e00656 [View Article] [PubMed]
     [Google Scholar]
  29. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 1995; 33:2233–2239 [View Article] [PubMed]
     [Google Scholar]
  30. Calvez S, Fournel C, Douet D-G, Daniel P. Pulsed-field gel electrophoresis and multi locus sequence typing for characterizing genotype variability of Yersinia ruckeri isolated from farmed fish in France. Vet Res 2015; 46:73 [View Article] [PubMed]
     [Google Scholar]
  31. Huang W, Li L, Myers JR, Marth GT. ART: a next-generation sequencing read simulator. Bioinformatics 2012; 28:593–594 [View Article] [PubMed]
     [Google Scholar]
  32. Sarovich DS, Price EP. SPANDx: a genomics pipeline for comparative analysis of large haploid whole genome re-sequencing datasets. BMC Res Notes 2014; 7:618 [View Article] [PubMed]
     [Google Scholar]
  33. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article]
     [Google Scholar]
  34. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article] [PubMed]
     [Google Scholar]
  35. Quinlan AR, Clark RA, Sokolova S, Leibowitz ML, Zhang Y et al. Genome-wide mapping and assembly of structural variant breakpoints in the mouse genome. Genome Res 2010; 20:623–635 [View Article] [PubMed]
     [Google Scholar]
  36. Danecek P, Auton A, Abecasis G, Albers CA, Banks E et al. The variant call format and VCFtools. Bioinformatics 2011; 27:2156–2158 [View Article] [PubMed]
     [Google Scholar]
  37. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010; 20:1297–1303 [View Article] [PubMed]
     [Google Scholar]
  38. Swofford DL. PAUP*. Phylogenetic analysis using parsimony (*and other methods), V4.0a168. Sunderland, MA: Sinauer Associates; 2003
  39. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 2012; 6:80–92 [View Article] [PubMed]
     [Google Scholar]
  40. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 2004; 14:1394–1403 [View Article] [PubMed]
     [Google Scholar]
  41. Alikhan N-F, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011; 12:402 [View Article] [PubMed]
     [Google Scholar]
  42. Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ et al. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol 2018; 4:vey016 [View Article] [PubMed]
     [Google Scholar]
  43. Holt K, Kenyon JJ, Hamidian M, Schultz MB, Pickard DJ et al. Five decades of genome evolution in the globally distributed, extensively antibiotic-resistant Acinetobacter baumannii global clone 1. Microb Genom 2016; 2:e000052 [View Article] [PubMed]
     [Google Scholar]
  44. Holt K, Kenyon JJ, Hamidian M, Schultz MB, Pickard DJ et al. Five decades of genome evolution in the globally distributed, extensively antibiotic-resistant Acinetobacter baumannii global clone 1. Microb Genom 2016; 2:e000052 [View Article] [PubMed]
     [Google Scholar]
  45. Germer S, Holland MJ, Higuchi R. High-throughput SNP allele-frequency determination in pooled DNA samples by kinetic PCR. Genome Res 2000; 10:258–266 [View Article] [PubMed]
     [Google Scholar]
  46. Price EP, Matthews MA, Beaudry JA, Allred JL, Schupp JM et al. Cost-effective interrogation of single nucleotide polymorphisms using the mismatch amplification mutation assay and capillary electrophoresis. Electrophoresis 2010; 31:3881–3888 [View Article] [PubMed]
     [Google Scholar]
  47. Birdsell DN, Pearson T, Price EP, Hornstra HM, Nera RD et al. Melt analysis of mismatch amplification mutation assays (Melt-MAMA): a functional study of a cost-effective SNP genotyping assay in bacterial models. PLoS One 2012; 7:e32866 [View Article] [PubMed]
     [Google Scholar]
  48. Hézard N, Cornillet P, Droullé C, Gillot L, Potron G et al. Factor V Leiden: detection in whole blood by ASA PCR using an additional mismatch in antepenultimate position. Thromb Res 1997; 88:59–66 [View Article] [PubMed]
     [Google Scholar]
  49. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
     [Google Scholar]
  50. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008; 18:821–829 [View Article] [PubMed]
     [Google Scholar]
  51. Assefa S, Keane TM, Otto TD, Newbold C, Berriman M. ABACAS: algorithm-based automatic contiguation of assembled sequences. Bioinformatics 2009; 25:1968–1969 [View Article] [PubMed]
     [Google Scholar]
  52. Tsai IJ, Otto TD, Berriman M. Improving draft assemblies by iterative mapping and assembly of short reads to eliminate gaps. Genome Biol 2010; 11:R41 [View Article] [PubMed]
     [Google Scholar]
  53. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011; 27:578–579 [View Article]
     [Google Scholar]
  54. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano WJB. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011; 27:578–579 [View Article] [PubMed]
     [Google Scholar]
  55. Boetzer M, Pirovano W. Toward almost closed genomes with GapFiller. Genome Biol 2012; 13:R56 [View Article] [PubMed]
     [Google Scholar]
  56. Nadalin F, Vezzi F, Policriti A. GapFiller: a de novo assembly approach to fill the gap within paired reads. BMC Bioinformatics 2012; 13:14 [View Article] [PubMed]
     [Google Scholar]
  57. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 2014; 9:e112963 [View Article] [PubMed]
     [Google Scholar]
  58. Seemann TJB. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
     [Google Scholar]
  59. Couvin D, Bernheim A, Toffano-Nioche C, Touchon M, Michalik J et al. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res 2018; 46:W246–W251 [View Article] [PubMed]
     [Google Scholar]
  60. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article] [PubMed]
     [Google Scholar]
  61. Wattam AR, Abraham D, Dalay O, Disz TL, Driscoll T et al. PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res 2014; 42:D581–91 [View Article] [PubMed]
     [Google Scholar]
  62. Crispell J, Balaz D, Gordon SV. HomoplasyFinder: a simple tool to identify homoplasies on a phylogeny. Microb Genom 2019; 5: [View Article] [PubMed]
     [Google Scholar]
  63. Vera-Cabrera L, Ortiz-Lopez R, Elizondo-Gonzalez R, Ocampo-Candiani J. Complete genome sequence analysis of Nocardia brasiliensis HUJEG-1 reveals a saprobic lifestyle and the genes needed for human pathogenesis. PLoS One 2013; 8:e65425 [View Article] [PubMed]
     [Google Scholar]
  64. Sun J, Fang W, Ke B, He D, Liang Y et al. Inapparent Streptococcus agalactiae infection in adult/commercial tilapia. Sci Rep 2016; 6:26319 [View Article] [PubMed]
     [Google Scholar]
  65. Bakker HC den, Switt AIM, Cummings CA, Hoelzer K, Degoricija L et al. A whole-genome single nucleotide polymorphism-based approach to trace and identify outbreaks linked to A common Salmonella enterica subsp. enterica serovar Montevideo pulsed-field gel electrophoresis type. Appl Environ Microbiol 2011; 77:8648–8655 [View Article] [PubMed]
     [Google Scholar]
  66. Kwong JC, Mercoulia K, Tomita T, Easton M, Li HY et al. Prospective whole-genome sequencing enhances national surveillance of Listeria monocytogenes. J Clin Microbiol 2016; 54:333–342 [View Article] [PubMed]
     [Google Scholar]
  67. Lee K-I, Morita-Ishihara T, Iyoda S, Ogura Y, Hayashi T et al. A geographically widespread outbreak investigation and development of a rapid screening method using whole genome sequences of enterohemorrhagic Escherichia coli O121. Front Microbiol 2017; 8:701 [View Article] [PubMed]
     [Google Scholar]
  68. Seifert H, Dolzani L, Bressan R, van der Reijden T, van Strijen B et al. Standardization and interlaboratory reproducibility assessment of pulsed-field gel electrophoresis-generated fingerprints of Acinetobacter baumannii. J Clin Microbiol 2005; 43:4328–4335 [View Article] [PubMed]
     [Google Scholar]
  69. Uelze L, Grützke J, Borowiak M, Hammerl JA, Juraschek K et al. Typing methods based on whole genome sequencing data. One Health Outlook 2020; 2:3 [View Article] [PubMed]
     [Google Scholar]
  70. Nakada M. Capture-based aquaculture of yellowtail. In Lovatelli A, Holthus PF. eds Capture-Based Aquaculture Global Overview Rome: FAO Fisheries Technical Paper 2008. No. 508 FAO; pp 199–215
     [Google Scholar]
  71. Labrie L, Ng J, Tan Z, Komar C, Ho E et al. Nocardial infections in fish: an emerging problem in both freshwater and marine aquaculture systems in Asia. Diseases in Asian aquaculture VI Fish Health Section, Asian Fisheries Society, Manila 2008297–312
     [Google Scholar]
  72. Davis-Scibienski C, Beaman BL. Interaction of Nocardia asteroides with rabbit alveolar macrophages: association of virulence, viability, ultrastructural damage, and phagosome-lysosome fusion. Infect Immun 1980; 28:610–619 [View Article] [PubMed]
     [Google Scholar]
  73. Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA et al. An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Microbiol 2015; 13:722–736 [View Article] [PubMed]
     [Google Scholar]
  74. Newsom S, Parameshwaran HP, Martin L, Rajan R. The CRISPR-cas mechanism for adaptive immunity and alternate bacterial functions fuels diverse biotechnologies. Front Cell Infect Microbiol 2020; 10:619763 [View Article] [PubMed]
     [Google Scholar]
  75. Meaden S, Biswas A, Arkhipova K, Morales SE, Dutilh BE et al. High viral abundance and low diversity are associated with increased CRISPR-Cas prevalence across microbial ecosystems. Curr Biol 2022; 32:220–227 [View Article] [PubMed]
     [Google Scholar]
  76. Russel J, Pinilla-Redondo R, Mayo-Muñoz D, Shah SA, Sørensen SJ. CRISPRcastyper: automated identification, annotation, and classification of CRISPR-cas loci. CRISPR J 2020; 3:462–469 [View Article] [PubMed]
     [Google Scholar]
  77. Zhang Q, Ye Y. Not all predicted CRISPR-Cas systems are equal: isolated cas genes and classes of CRISPR like elements. BMC Bioinformatics 2017; 18:1–12 [View Article] [PubMed]
     [Google Scholar]
  78. Zhang M, Bi C, Wang M, Fu H, Mu Z et al. Analysis of the structures of confirmed and questionable CRISPR loci in 325 Staphylococcus genomes. J Basic Microbiol 2019; 59:901–913 [View Article] [PubMed]
     [Google Scholar]
  79. Shmakov SA, Utkina I, Wolf YI, Makarova KS, Severinov KV et al. CRISPR arrays away from cas genes. CRISPR J 2020; 3:535–549 [View Article]
     [Google Scholar]
  80. Tanmoy AM, Saha C, Sajib MSI, Saha S, Komurian-Pradel F et al. CRISPR-cas diversity in clinical Salmonella enterica serovar Typhi isolates from South Asian countries. Genes 2020; 11:E1365 [View Article] [PubMed]
     [Google Scholar]
  81. de Oliveira Luz AC, da Silva Junior WJ, do Nascimento Junior JB, da Silva JMA, de Queiroz Balbino V et al. Genetic characteristics and phylogenetic analysis of Brazilian clinical strains of Pseudomonas aeruginosa harboring CRISPR/Cas systems. Curr Genet 2021; 67:663–672 [View Article] [PubMed]
     [Google Scholar]
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Comparative genomics of Nocardia seriolae reveals recent importation and subsequent widespread dissemination in mariculture farms in the South Central Coast region, Vietnam
M Gen 8, 000845 (2022); https://doi.org/10.1099/mgen.0.000845
/content/journal/mgen/10.1099/mgen.0.000845
/content/journal/mgen/10.1099/mgen.0.000845
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