Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-27T10:56:19.221Z Has data issue: false hasContentIssue false
  • English
  • Français

Whole-genome amplification: a useful approach to characterize new genes in unculturable protozoan parasites such as Bonamia exitiosa

Published online by Cambridge University Press:  18 August 2015

MARIA PRADO-ALVAREZ ,
YANN COURALEAU ,
BRUNO CHOLLET ,
DELPHINE TOURBIEZ  and
ISABELLE ARZUL
MARIA PRADO-ALVAREZ
Affiliation:
Laboratoire de Génétique et Pathologie des Mollusques Marins, IFREMER, Avenue de Mus de Loup, 17390 La Tremblade, France
YANN COURALEAU
Affiliation:
Laboratoire de Génétique et Pathologie des Mollusques Marins, IFREMER, Avenue de Mus de Loup, 17390 La Tremblade, France
BRUNO CHOLLET
Affiliation:
Laboratoire de Génétique et Pathologie des Mollusques Marins, IFREMER, Avenue de Mus de Loup, 17390 La Tremblade, France
DELPHINE TOURBIEZ
Affiliation:
Laboratoire de Génétique et Pathologie des Mollusques Marins, IFREMER, Avenue de Mus de Loup, 17390 La Tremblade, France
ISABELLE ARZUL*
Affiliation:
Laboratoire de Génétique et Pathologie des Mollusques Marins, IFREMER, Avenue de Mus de Loup, 17390 La Tremblade, France
*
* Corresponding author. Laboratoire de Génétique et Pathologie des Mollusques Marins, IFREMER, Avenue de Mus de Loup, 17390 La Tremblade, France. E-mail: iarzul@ifremer.fr
Get access Rights & Permissions [Opens in a new window]

Summary

Bonamia exitiosa is an intracellular parasite (Haplosporidia) that has been associated with mass mortalities in oyster populations in the Southern hemisphere. This parasite was recently detected in the Northern hemisphere including Europe. Some representatives of the Bonamia genus have not been well categorized yet due to the lack of genomic information. In the present work, we have applied Whole-Genome Amplification (WGA) technique in order to characterize the actin gene in the unculturable protozoan B. exitiosa. This is the first protein coding gene described in this species. Molecular analysis revealed that B. exitiosa actin is more similar to Bonamia ostreae actin gene-1. Actin phylogeny placed the Bonamia sp. infected oysters in the same clade where the herein described B. exitiosa actin resolved, offering novel information about the classification of the genus. Our results showed that WGA methodology is a promising and valuable technique to be applied to unculturable protozoans whose genomic material is limited.

Keywords

Bonamia exitiosaBonamia ostreaeactinHaplosporidiaWhole-Genome Amplification
Type
Research Article
Information
Parasitology , Volume 142 , Issue 12 , October 2015 , pp. 1523 - 1534
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abollo, E., Ramilo, A., Casas, S. M., Comesaña, P., Cao, A., Carballal, M. J. and Villalba, A. (2008). First detection of the protozoan parasite Bonamia exitiosa (Haplosporidia) infecting flat oyster Ostrea edulis grown in European waters. Aquaculture 274, 201–207.Google Scholar
Arzul, I., Omnes, E., Robert, M., Chollet, B., Joly, J. P., Miossec, L., Franand, C. and Garcia C., (2010). Distribution of Bonamia exitiosa in flat oyster Ostrea edulis populations in France. Aquaculture 2010, San Diego, California.Google Scholar
Arzul, I., Aranguren, R., Arcangeli, G., Chesslet, D., Engelsma, M., Figueras, A., Garcia, C., Geoghegan, F., Magnabosco, C. and Stone, D. (2011). Distribution of Bonamia exitiosa in flat oyster Ostrea edulis populations in Europe. In 15th EAFP International Conferences on Diseases of Fish and Shellfish, Split, Croatia.Google Scholar
Bouzid, M., Heavens, D., Elwin, K., Chalmers, R. M., Hadfield, S. J., Hunter, P. R. and Tyler, K. M. (2010). Whole genome amplification (WGA) for archiving and genotyping of clinical isolates of Cryptosporidium species. Parasitology 137, 27–36.Google Scholar
Burki, F., Kudryavtsev, A., Matz, M. V., Aglyamova, G. V., Bulman, S., Fiers, M., Keeling, P. J. and Pawlowski, J. (2010). Evolution of Rhizaria: new insights from phylogenomic analysis of uncultivated protists. BMC Evolutionary Biology 10, 377.CrossRefGoogle ScholarPubMed
Burki, F., Corradi, N., Sierra, R., Pawlowski, J., Meyer, G. R., Abbott, C. L., and Keeling, P. J. (2013). Phylogenomics of the ‘amitochondriate’ intracellular parasite Mikrocytos mackini reveals first evidence for a mitosome in Rhizaria. Current Biology 23, 1541–1547.CrossRefGoogle Scholar
Burreson, E. M., Stokes, N. A., Carnegie, R. B., and Bishop, M. J. (2004). Bonamia sp. (Haplosporidia) found in nonnative oysters Crassostrea ariakensis in Bogue Sound, North Carolina. Journal of Aquatic Animal Health 16, 1–9.CrossRefGoogle Scholar
Campalans, M., Rojas, P. and Gonzalez, M. (2000). Haemocytic parasitosis in the farmed oyster Tiostrea chilensis . Bulletin European Association of Fish Pathologists 20, 31–33.Google Scholar
Carnegie, R. B., Barber, B. J., Culloty, S. C., Figueras, A. J. and Distel, D. L. (2000). Development of a PCR assay for detection of the oyster pathogen Bonamia ostreae and support for its inclusion in the Haplosporidia. Diseases of Aquatic Organisms 42, 199–206.CrossRefGoogle ScholarPubMed
Carnegie, R. B., Burreson, E. M., Hine, P. M., Stokes, N. A., Audemard, C., Bishop, M. J. and Peterson, C. H. (2006). Bonamia perspora n. sp. (Haplosporidia), a parasite of the oyster Ostreola equestris, is the first Bonamia species known to produce spores. Journal of Eukaryotic Microbiology 53, 232–245.Google Scholar
Carnegie, R. B., Hill, K. M., Stokes, N. A. and Burreson, E. M. (2014). The haplosporidian Bonamia exitiosa is present in Australia, but the identity of the parasite described as Bonamia (formerly Mikrocytos) roughleyi is uncertain. Journal of Invertebrate Pathology 115, 33–40.Google Scholar
Carrasco, N., Villalba, A., Andree, K. B., Engelsma, M. Y., Lacuesta, B., Ramilo, A., Gairín, I. and Furones, M. D. (2012). Bonamia exitiosa (Haplosporidia) observed infecting the European flat oyster Ostrea edulis cultured on the Spanish Mediterranean coast. Journal of Invertebrate Pathology 110, 307–313.CrossRefGoogle ScholarPubMed
Carret, C. K., Horrocks, P., Konfortov, B., Winzeler, E., Qureshi, M., Newbold, C. and Ivens, A. (2005). Microarray-based comparative genomic analyses of the human malaria parasite Plasmodium falciparum using Affymetrix arrays. Molecular and Biochemical Parasitology 144, 177–186.Google Scholar
Cavalier-Smith, T. (2002). The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. International Journal of Systematic and Evolutionary Microbiology 52, 297–354.Google Scholar
Cavalier-Smith, T. and Chao, E. E. (2003). Phylogeny and classification of phylum Cercozoa (Protozoa). Protist 154, 341–358.Google Scholar
Cochennec-Laureau, N., Le Roux, F., Berthe, F. and Gerard, A. (2000). Detection of Bonamia ostreae based on small subunit ribosomal probe. Journal of Invertebrate Pathology 76, 26–32.Google Scholar
Cochennec-Laureau, N., Reece, K. S., Berthe, F. C. J. and Hine, P. M. (2003). Mikrocytos roughleyi taxonomic affiliation leads to the genus Bonamia (Haplosporidia). Diseases of Aquatic Organisms 54, 209–217.Google Scholar
Corbeil, S., Arzul, I., Robert, M., Berthe, F. C. J., Besnard-Cochennec, N. and Crane, M. S. J. (2006). Molecular characterization of an Australian isolate of Bonamia exitiosa . Diseases of Aquatic Organisms 71, 81–85.Google Scholar
Cranfield, H. J., Dunn, A., Doonan, I. J. and Michael, K. P. (2005). Bonamia exitiosa epizootic in Ostrea chilensis from Foveaux Strait, southern New Zealand between 1986 and 1992. ICES Journal of Marine Science 62, 3–13.Google Scholar
Doonan, I. J., Cranfield, H. J. and Jones, J. B. (1994). Catastrophic reduction of the oyster, Tiostrea chilensis (Bivalvia: Ostreidae), in Foveaux Strait, New Zealand, due to infestation by the protistan Bonamia sp. New Zealand Journal of Marine and Freshwater Research 28, 335–344.Google Scholar
Fairbrother, K. S., Hopwood, A. J., Lockley, A. K. and Bardsley, R. G. (1998). The actin multigene family and livestock speciation using the polymerase chain reaction. Animal Biotechnology 9, 89–100.CrossRefGoogle ScholarPubMed
Fyrberg, E. A., Kindle, K. L., Davidson, N. and Kindle, K. L. (1980). The actin genes of Drosophila: a dispersed multigene family. Cell 19, 365–378.Google Scholar
Hill, K. M., Carnegie, R. B., Aloui-Bejaoui, N., El Gharsalli, R., White, D. M., Stokes, N. A. and Burreson, E. M. (2010). Observation of a Bonamia sp. infecting the oyster Ostrea stentina in Tunisia, and a consideration of its phylogenetic affinities. Journal of Invertebrate Pathology 103, 179–185.Google Scholar
Hine, P. M., Cochennec-Laureau, N. and Berthe, F. C. J. (2001). Bonamia exitiosus n. sp. (Haplosporidia) infecting flat oysters Ostrea chilensis (Philippi) in New Zealand. Diseases of Aquatic Organisms 47, 63–72.Google Scholar
Keeling, P. J. (2001). Foraminifera and Cercozoa are related in actin phylogeny: Two orphans find a home? Molecular Biology and Evolution 18, 1551–1557.Google Scholar
Kim, S., Bachvaroff, T. R., Hand, S. M. and Delwiche, C. F. (2011). Dynamics of actin evolution in Dinoflagellates. Molecular Biology and Evolution 28, 1469–1480.CrossRefGoogle ScholarPubMed
Korfhage, C., Fisch, E., Fricke, E., Baedker, S. and Loeffert, D. (2013). Whole-genome amplification of single-cell genomes for next-generation sequencing. Current Protocols in Molecular Biology 104, 7.Google Scholar
Korn, E. D., Carlier, M. F. and Pantaloni, D. (1987). Actin polymerization and ATP hydrolysis. Science 238, 638–644.Google Scholar
Leander, B. S. and Keeling, P. J. (2004). Early evolutionary history of Dinoflagellates and Apicomplexans (Alveolata) as inferred from HSP90 and actin phylogenies. Journal of Phycology 40, 341–350.Google Scholar
Lohrmann, K. B., Hine, P. M. and Campalans, M. (2009). Ultrastructure of Bonamia sp. in Ostrea chilensis in Chile. Diseases of Aquatic Organisms 85, 199–208.CrossRefGoogle ScholarPubMed
Longet, D., Burki, F., Flakowski, J., Berney, C., Polet, S., Fahrni, J. and Pawlowski, J. (2004). Multigene evidence for close evolutionary relations between Gromia and Foraminifera. Acta Protozoologica 43, 303–311.Google Scholar
Lonshaw, M., Stone, D. M., Wood, G., Green, M. J. and White, P. (2013). Detection of Bonamia exitiosa (Haplosporidia) in European flat oysters Ostrea edulis cultivated in mainland Britain. Diseases of Aquatic Organisms 106, 173–179.Google Scholar
López-Flores, I., Suárez-Santiago, V. N., Longet, D., Saulnier, D., Chollet, B. and Arzul, I. (2007). Characterization of actin genes in Bonamia ostreae and their application to phylogeny of the Haplosporidia. Parasitology 134, 1941–1948.Google Scholar
McLean, J. S., Lombardo, M. J., Ziegler, M. G., Novotny, M., Yee-Greenbaum, J., Badger, J. H., Tesler, G., Nurk, S., Lesin, V., Brami, D., Hall, A. P., Edlund, A., Allen, L. Z., Durkin, S., Reed, S., Torriani, F., Nealson, K. H., Pevzner, P. A., Friedman, R., Venter, J. C. and Lasken, R. S. (2013). Genome of the pathogen Porphyromonas gingivalis recovered from a biofilm in a hospital sink using a high-throughput single-cell genomics platform. Genome Research 23, 867–877.Google Scholar
Meuriot, E. and Grizel, H. (1984). Note sur l'impact économique des maladies de l'huître plate en Bretagne. Rapports Techniques de l'Institut Scientifique et Technique des Péches Maritimes 12, 1–20.Google Scholar
Mialhe, E., Bachère, E., Chagot, D. and Grizel, H. (1988). Isolation and purification of the protozoan Bonamia ostreae (Pichot et al, 1980), a parasite affecting the flat oyster Ostrea edulis L. Aquaculture 71, 293–299.Google Scholar
Morrison, L. J., Mccormack, G., Sweeney, L., Likeufack, A. C. L., Truc, P., Turner, C. M., Tait, A. and Macleod, A. (2007). Use of multiple displacement amplification to increase the detection and genotyping of trypanosoma species samples immobilized on FTA filters. The American Journal of Tropical Medicine and Hygiene 76, 1132–1137.Google Scholar
Narcisi, V., Arzul, I., Cargini, D., Mosca, F., Calzetta, A., Traversa, D., Robert, M., Joly, J. P., Chollet, B., Renault, T. and Tiscar, P. G. (2010). Detection of Bonamia ostreae and B. exitiosa (Haplosporidia) in Ostrea edulis from the Adriatic Sea (Italy). Diseases of Aquatic Organisms 89, 79–85.Google Scholar
Nelson, J. R. (2014). Random-primed, Phi29 DNA polymerase-based whole genome amplification. Current Protocols in Molecular Biology 105, 13.Google Scholar
OIE (2013). Aquatic Animal Health Code. http://www.oie.int/en/international-standard-setting/aquatic-code/access-online/ Google Scholar
Pamp, S. J., Harrington, E. D., Quake, S. R., Relman, D. A. and Blainey, P. C. (2012). Single-cell sequencing provides clues about the host interactions of segmented filamentous bacteria (SFB). Genome Research 22, 1107–1119.Google Scholar
Pan, X., Urban, A. E., Palejev, D., Schulz, V., Grubert, F., Hu, Y., Snyder, M. and Weissman, S. M. (2008). A procedure for highly specific, sensitive, and unbiased whole-genome amplification. Proceedings of the National Academy of Sciences 105, 15499–15504.Google Scholar
Prado-Alvarez, M., Chollet, B., Couraleau, Y., Morga, B. and Arzul, I. (2013). Heat shock protein 90 of Bonamia ostreae: Characterization and possible correlation with infection of the flat oyster, Ostrea edulis . Journal of Eukaryotic Microbiology 60, 257–266.Google Scholar
Reece, K. S., Siddall, M. E., Stokes, N. A. and Burreson, E. M. (2004). Molecular phylogeny of the haplosporidia based on two independent gene sequences. Journal of Parasitology 90, 1111–1122.CrossRefGoogle ScholarPubMed
Robert, M., Garcia, C., Chollet, B., López-Flores, I., Ferrand, S. F. C., Joly, J. P. and Arzul, I. (2009). Molecular detection and quantification of the protozoan Bonamia ostreae in the flat oyster, Ostrea edulis . Molecular and Cellular Probes 23, 264–271.Google Scholar
Schafer, D. A., Cooper, J. A. (1995). Control of actin assembly at filament ends. Annual Review of Cell and Developmental Biology 11, 497–518.Google Scholar
Schutt, C. E., Myslik, J. C., Rozycki, M. D., Goonesekere, N. C. W. and Lindberg, U. (1993). The structure of crystalline profilin–β-actin. Nature 365, 810–816.Google Scholar
Schwartz, R. J. and Rotblum, K. N. (1981). Gene switching in myogenesis: differential expression of the chicken actin multigene family. Biochemistry 20, 4122–4129.Google Scholar
Sehring, I. M., Mansfeld, J., Reiner, C., Wagner, E., Plattner, H. and Kissmehl, R. (2007). The actin multigene family of Paramecium tetraurelia . BMC Genomics 8, 82.Google Scholar
Seth-Smith, H. M., Harris, S. R., Skilton, R. J., Radebe, F. M., Golparian, D., Shipitsyna, E., Duy, P. T., Scott, P., Cutcliffe, L. T., O'Neill, C., Parmar, S., Pitt, R., Baker, S., Ison, C. A., Marsh, P., Jalal, H., Lewis, D. A., Unemo, M., Clarke, I. N., Parkhill, J. and Thomson, N. R. (2013). Whole-genome sequences of Chlamydia trachomatis directly from clinical samples without culture. Genome Research 23, 855–866.CrossRefGoogle ScholarPubMed
Sheterline, P., Clayton, J. and Sparrow, J. C. (1995). Actin. In Protein Profile (ed. Sheterline, P.), Vol. 2, pp. 1–103. Oxford University Press, Oxford, UK.Google Scholar
Spits, C., Le Caignec, C., De Rycke, M., Van Haute, L., Van Steirteghem, A., Liebaers, I. and Sermon, K. (2006). Whole-genome multiple displacement amplification from single cells. Nature Protocols 1, 1965–1970.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using máximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.Google Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality tools. Nucleic Acids Research 25, 4876–4882.Google Scholar
Wesseling, J. G., Smits, M. A. and Schoenmakers, J. G. G. (1988). Extremely diverged actin proteins in Plasmodium falciparum . Molecular and Biochemical Parasitology 30, 143–154.Google Scholar
Young, N. D., Jex, A. R., Li, B., Liu, S., Yand, L., Xiong, X., Li, Y., Cantacessi, C., Hall, R. S., Xu, X., Chen, F., Wu, X., Zerlotini, A., Oliveira, G., Hofmann, A., Zhang, G., Fang, X., Kang, Y., Campbell, B. E., Loukas, A., Ranganathan, S., Rollinson, D., Rinaldi, G., Brindley, P. J., Yang, H., Wang, J., Wang, J., Gasser, R. B. (2012). Whole-genome sequence of Schistosoma haematobium . Nature Genetics 44, 221–225.Google Scholar