Advertisement

Hydrobiologia

, Volume 805, Issue 1, pp 221–230 | Cite as

Occurrence of the planktonic bloom-forming marine diatom Chaetoceros tenuissimus Meunier and its infectious viruses in western Japan

Primary Research Paper

Abstract

The genus Chaetoceros is among the most species-rich marine planktonic diatoms. Most Chaetoceros are considered important primary producers in various marine environments, but because of their small size, we know little about their ecology and distribution. Therefore, from 2008 to 2012, we examined the occurrence of C. tenuissimus Meunier, one of the smallest members in the genus, and its infectious viruses in western Japanese coastal waters. Using real-time quantitative PCR, we found that C. tenuissimus was widely detected throughout our study sites, with a maximum concentration of 2.4 × 107 cells/l in May 2012. Sediment analysis revealed that C. tenuissimus resting-stage cells were present at potentially high levels, despite its infectious viruses being detected in the same region. The present study suggests that C. tenuissimus remains highly productive even when surrounded by its infectious viruses. This tolerance to viral infection, along with the diatom’s fast growth rate, suggests that C. tenuissimus might play an important role in maintaining the growth of important filter feeders.

Keywords

Algal viruses Primary producers Marine algae Real-time quantitative PCR Resting-stage cells 

Notes

Acknowledgements

This study was supported by KAKENHI (16K14963) and grants for Scientific Research on Innovative Areas (16H06429, 16K21723, 16H06437) from the Ministry of Education, Culture, Science, Sports and Technology (MEXT) of Japan.

Author contributions

Y.T. wrote the main text and prepared all figures and tables. All authors collected data, conducted experiments, and reviewed the manuscript.

Compliance with ethical standard

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10750_2017_3306_MOESM1_ESM.pptx (304 kb)
Supplementary material 1 (PPTX 304 kb)
10750_2017_3306_MOESM2_ESM.docx (51 kb)
Supplementary material 2 (DOCX 50 kb)

References

  1. Baytut, Ö., Ø. Moestrup, N. Lundholm & A. Gönülol, 2013. Contributions to the Diatom flora of the Black Sea from ultrastructural and molecular studies: new records of Skeletonema marinoi, Pseudo-nitzschia pungens var. aveirensis and Chaetoceros tenuissimus for the marine flora of Turkey. Nova Hedwigia 96: 427–444.CrossRefGoogle Scholar
  2. Bettarel, Y., J. Kan, K. Wang, K. Williamson, S. Cooney, S. Ribblett, F. Chen, E. Wommack & W. Coats, 2005. Isolation and preliminary characterisation of a small nuclear inclusion virus infecting the diatom Chaetoceros c.f. gracilis. Aquatic Microbial Ecology 40: 103–114.Google Scholar
  3. Collier, A. & A. Murphy, 1962. Very small diatoms: preliminary notes and description of Chaetoceros galvestonensis. Science 136: 780–781.CrossRefPubMedGoogle Scholar
  4. Culley, A. I., J. A. Mueller, M. Belcaid, E. M. Wood-Charlson, G. Poisson & G. F. Steward, 2014. The characterization of RNA viruses in tropical seawater using targeted PCR and metagenomics. mBio 5: e01210–e01214.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Enright, C., G. Newkirk, J. Craigie & J. Castell, 1986a. Evaluation of phytoplankton as diets for juvenile Ostrea edulis L. Journal of Experimental Marine Biology and Ecology 96: 1–13.CrossRefGoogle Scholar
  6. Enright, C., G. Newkirk, J. Craigie & J. Castell, 1986b. Growth of juvenile Ostrea edulis L. fed Chaetoceros gracilis Schütt of varied chemical composition. Journal of Experimental Marine Biology and Ecology 96: 15–26.CrossRefGoogle Scholar
  7. Frada, M., I. Probert, M. J. Allen, W. H. Wilson & C. de Vargas, 2008. The “Cheshire Cat” escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection. Proceedings of the National Academy of Sciences of the United States of America 105: 15944–15949.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Gustavsen, J. A., D. M. Winget, X. Tian & C. A. Suttle, 2014. High temporal and spatial diversity in marine RNA viruses implies that they have an important role in mortality and structuring plankton communities. Frontiers in Microbiology 5: 703.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Hustedt, F., 1930. Bacillariophyta (Diatomeae). Die Susswasser Flora Mitteleuropas 10: 466.Google Scholar
  10. Imai, I., S. Itakura, Y. Matsuyama & M. Yamaguchi, 1996. Selenium requirement for growth of a novel red tide flagellate Chattonella verruculosa (Raphidophyceae) in culture. Fisheries Science 62: 834–835.CrossRefGoogle Scholar
  11. Ishii, K.-I., M. Iwataki, K. Matsuoka & I. Imai, 2011. Proposal of identification criteria for resting spores of Chaetoceros species (Bacillariophyceae) from a temperate coastal sea. Phycologia 50: 351–362.CrossRefGoogle Scholar
  12. Itakura, S., 2000. Physiological ecology of the resting stage cells of coastal planktonic diatoms. Bulletin of Fisheries and Environment of Inland Sea 2: 67–130.Google Scholar
  13. Kaspar, H. F., E. F. Keys, N. King, K. F. Smith, A. Kesarcodi-Watson & M. R. Miller, 2014. Continuous production of Chaetoceros calcitrans in a system suitable for commercial hatcheries. Aquaculture 420: 1–9.CrossRefGoogle Scholar
  14. Kimura, K. & Y. Tomaru, 2014. Coculture with marine bacteria confers resistance to complete viral lysis of diatom cultures. Aquatic Microbial Ecology 73: 69–80.CrossRefGoogle Scholar
  15. Kimura, K. & Y. Tomaru, 2015. Discovery of two novel viruses expands the diversity of ssDNA and ssRNA viruses infecting a cosmopolitan marine diatom. Applied and Environmental Microbiology 81: 1120–1131.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Kooistra, W. H., D. Sarno, D. U. Hernández-Becerril, P. Assmy, C. Di Prisco & M. Montresor, 2010. Comparative molecular and morphological phylogenetic analyses of taxa in the Chaetocerotaceae (Bacillariophyta). Phycologia 49: 471–500.CrossRefGoogle Scholar
  17. Lawrence, J., 2005. Viral contamination of algal cultures. In Anderson, R. A. (ed.), Algal Culturing Techniques. Academic Press, Amsterdam: 365–388.Google Scholar
  18. McDaniel, L. D., K. Rosario, M. Breitbart & J. H. Paul, 2014. Comparative metagenomics: natural populations of induced prophages demonstrate highly unique, lower diversity viral sequences. Environmental Microbiology 16: 570–585.CrossRefPubMedGoogle Scholar
  19. Meunier, A., 1913. Microplankton de la mer Flamande. Hayez, imprimeur de l’Académie royale de Belgique, Bruxelles.Google Scholar
  20. Miranda, J. A., A. I. Culley, C. R. Schvarcz & G. F. Steward, 2016. RNA viruses as major contributors to Antarctic virioplankton. Environmental Microbiology 18: 3714–3727.CrossRefPubMedGoogle Scholar
  21. Mojica, K. D. & C. P. Brussaard, 2014. Factors affecting virus dynamics and microbial host-virus interactions in marine environments. FEMS Microbiology Ecology 89: 495–515.Google Scholar
  22. Montresor, M., C. Di Prisco, D. Sarno, F. Margiotta & A. Zingone, 2013. Diversity and germination patterns of diatom resting stages at a coastal Mediterranean site. Marine Ecology Progress Series 484: 79–95.CrossRefGoogle Scholar
  23. Nelson, D. M., P. Treguer, M. A. Brzezinski, A. Leynaert & B. Queguiner, 1995. Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochemical Cycles 9: 359–372.CrossRefGoogle Scholar
  24. Nishihara, T., N. Kurano & S. Shinoda, 1986. Calculation of most probable number for enumeration of bacteria on microcomputer. Eisei Kagaku 32: 226–228. (in Japanese with English abstract)CrossRefGoogle Scholar
  25. Raven, J. A. & A. M. Waite, 2004. The evolution of silicification in diatoms: inescapable sinking and sinking as escape? New Phytologist 162: 45–61.CrossRefGoogle Scholar
  26. Rines, J. B. E. & P. E. Hargraves, 1988. The Chaetoceros Ehrenberg (Bacillariophyceae) flora of Narragansett Bay, Rhode Island, USA. Bibliotheca Phycologica 79: 196.Google Scholar
  27. Sar, E. A., D. U. Hernández-Becerril & I. Sunesen, 2002. A morphological study of Chaetoceros tenuissimus Meunier, a little-known planktonic diatom, with a discussion of the section Simplicia, subgenus Hyalochaete. Diatom Research 17: 327–335.CrossRefGoogle Scholar
  28. Sarthou, G., K. R. Timmermans, S. Blain & P. Treguer, 2005. Growth physiology and fate of diatoms in the ocean: a review. Journal of Sea Research 53: 25–42.CrossRefGoogle Scholar
  29. Shirai, Y., Y. Tomaru, Y. Takao, H. Suzuki, T. Nagumo & K. Nagasaki, 2008. Isolation and characterization of a single-stranded RNA virus infecting the marine planktonic diatom Chaetoceros tenuissimus Meunier. Applied and Environmental Microbiology 74: 4022–4027.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Suttle, C. A., 1993. Enumeration and isolation of viruses. In Kemp, P. F., E. Sherr & J. J. Cole (eds), Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton: 121–137.Google Scholar
  31. Takano, H., 1968. On the diatom Chaetoceros calcitrans (Paulsen) emend. and its dwarf form pumilus forma nov. Bulletin Tokai Regional Fisheries Research Laboratory 100: 35–43.Google Scholar
  32. Tomaru, Y., K. Tarutani, M. Yamaguchi & K. Nagasaki, 2004. Quantitative and qualitative impacts of viral infection on Heterosigma akashiwo (Raphidophyceae) population during a bloom in Hiroshima Bay, Japan. Aquatic Microbial Ecology 34: 227–238.CrossRefGoogle Scholar
  33. Tomaru, Y., N. Hata, T. Masuda, M. Tsuji, K. Igata, Y. Masuda, T. Yamatogi, M. Sakaguchi & K. Nagasaki, 2007. Ecological dynamics of the bivalve-killing dinoflagellate Heterocapsa circularisquama and its infectious viruses in different locations of western Japan. Environmental Microbiology 9: 1376–1383.CrossRefPubMedGoogle Scholar
  34. Tomaru, Y., Y. Shirai, H. Suzuki, T. Nagumo & K. Nagasaki, 2008. Isolation and characterization of a new single-stranded DNA virus infecting the cosmopolitan marine diatom Chaetoceros debilis. Aquatic Microbial Ecology 50: 103–112.CrossRefGoogle Scholar
  35. Tomaru, Y., H. Mizumoto & K. Nagasaki, 2009. Virus resistance in the toxic bloom-forming dinoflagellate Heterocapsa circularisquama to single-stranded RNA virus infection. Environmental Microbiology 11: 2915–2923.CrossRefPubMedGoogle Scholar
  36. Tomaru, Y., N. Fujii, S. Oda, K. Toyoda & K. Nagasaki, 2011. Dynamics of diatom viruses on the western coast of Japan. Aquatic Microbial Ecology 63: 223–230.CrossRefGoogle Scholar
  37. Tomaru, Y., K. Kimura & H. Yamaguchi, 2014. Temperature alters algicidal activity of DNA and RNA viruses infecting Chaetoceros tenuissimus. Aquatic Microbial Ecology 73: 171–183.CrossRefGoogle Scholar
  38. Tomaru, Y., K. Toyoda & K. Kimura, 2015. Marine diatom viruses and their hosts: Resistance mechanisms and population dynamics. Perspectives in Phycology 2: 69–81.Google Scholar
  39. Toyoda, K., K. Nagasaki & Y. Tomaru, 2010. Application of real-time PCR assay for detection and quantification of bloom-forming diatom Chaetoceros tenuissimus Meunier. Plankton and Benthos Research 5: 56–61.CrossRefGoogle Scholar
  40. Waterbury, J. B. & F. W. Valois, 1993. Resistance to co-occurring phages enables marine synechococcus communities to coexist with cyanophages abundant in seawater. Applied and Environmental Microbiology 59: 3393–3399.PubMedPubMedCentralGoogle Scholar
  41. Werner, D., 1977. Introduction with a note on taxonomy. In Werner, D. (ed.), The Biology of Diatoms, Vol. 13. Blackwell Scientific Publications, Victoria: 1–23.Google Scholar
  42. Zingone, A., F. Natale, E. Biffali, M. Borra, G. Forlani & D. Sarno, 2006. Diversity in morphology, infectivity, molecular characteristics and induced host resistance between two viruses infecting Micromonas pusilla. Aquatic Microbial Ecology 45: 1–14.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Japan Fisheries Research and Education AgencyNational Research Institute of Fisheries and Environment of the Inland SeaHatsukaichiJapan
  2. 2.Department of BiologyNippon Dental UniversityTokyoJapan
  3. 3.Ariake Sea Research Project/Institute of Lowland and Marine ResearchSaga UniversitySagaJapan

Personalised recommendations