Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes

Abstract

The cyanobacterium Prochlorococcus1,2 is the dominant oxygenic phototroph in the tropical and subtropical regions of the world's oceans1,3,4. It can grow at a range of depths over which light intensities can vary by up to 4 orders of magnitude. This broad depth distribution has been hypothesized to stem from the coexistence of genetically different populations adapted for growth at high- and low-light intensities4,5,6. Here we report direct evidence supporting this hypothesis, which has been generated by isolating and analysing distinct co-occurring populations of Prochlorococcus at two locations in the North Atlantic. Co-isolates from the same water sample have very different light-dependent physiologies, one growing maximally at light intensities at which the other is completely photoinhibited. Despite this ecotypic differentiation, the co-isolates have 97% similarity in their 16S ribosomal RNA sequences, demonstrating that molecular microdiversity, commonly observed in microbial systems7,8,9,10,11,12 can be due to the coexistence of closely related, physiologically distinct populations. The coexistence and distribution of multiple ecotypes permits the survival of the population as a whole over a broader range of environmental conditions than would be possible for a homogeneous population.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Properties of the euphotic zone and flow cytometric signatures of the Prochlorococcus populations and isolates.
Figure 2: Growth and photosynthetic rate as a function of irradiance for the Prochlorococcus isolates shown in Fig. 1.
Figure 3: Phylogenetic relationships of Prochlorococcus and Synechococcus isolates and environmental sequences from the Sargasso Sea (‘SAR’) inferred from 16S rRNA sequences.

References

  1. 1

    Chisholm, S. W. et al. Anovel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334, 340–343 (1988).

    ADS  Article  Google Scholar 

  2. 2

    Chisholm, S. W. et al. Prochlorococcus marinus nov. gen. nov. sp.: an oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. Arch. Microbiol. 157, 297–300 (1992).

    CAS  Article  Google Scholar 

  3. 3

    Olson, R. J., Chisholm, S. W., Zettler, E. R., Altabet, M. A. & Dusenberry, J. A. Spatial and temporal distributions of prochlorophyte picoplankton in the North Atlantic Ocean. Deep Sea Res. 37, 1033–1051 (1990).

    ADS  Article  Google Scholar 

  4. 4

    Campbell, L. & Vaulot, D. Photosynthetic picoplankton community structure in the subtropical North Pacific Ocean near Hawaii (station ALOHA). Deep Sea Res. 40, 2043–2060 (1993).

    Article  Google Scholar 

  5. 5

    Goericke, R. & Repeta, D. J. Chlorophylls a and b and divinyl chlorophylls a and b in the open subtropical North Atlantic Ocean. Mar. Ecol. Prog. Ser. 101, 307–313 (1993).

    ADS  CAS  Article  Google Scholar 

  6. 6

    Moore, L. R., Goericke, R. & Chisholm, S. W. Comparative physiology of Synechococcus and Prochlorococcus: influence of light and temperature on growth, pigments, fluorescence and absorptive properties. Mar. Ecol. Prog. Ser. 116, 259–275 (1995).

    ADS  Article  Google Scholar 

  7. 7

    Giovannoni, S. J., Britschgi, T. B., Moyer, C. L. & Field, K. G. Genetic diversity in Sargasso Sea bacterioplankton. Nature 345, 60–63 (1990).

    ADS  CAS  Article  Google Scholar 

  8. 8

    Fuhrman, J. A., McCallum, K. & Davis, A. A. Phylogenetic diversity of subsurface marine microbial communities from the Atlantic and Pacific Oceans. Appl. Environ. Microbiol. 59, 1294–1302 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. 9

    Palenik, B. Cyanobacterial community structure as seen from RNA polymerase gene sequence analysis. Appl. Environ. Microbiol. 60, 3212–3219 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10

    DeLong, E. F., Wu, K. Y., Prèzelin, B. B. & Jovine, R. V. M. High abundance of Archaea in Antarctic marine picoplankton. Nature 371, 695–697 (1994).

    ADS  CAS  Article  Google Scholar 

  11. 11

    Ward, D., Weller, M. R. & Bateson, M. M. 16S rRNA sequences reveal numerous uncultured microorganisms in a natural community. Nature 345, 63–65 (1990).

    ADS  CAS  Article  Google Scholar 

  12. 12

    Amann, R., Snaidr, J., Wagner, M., Ludwig, W. & Schleifer, K.-H. In situ visualization of high genetic diversity in a natural microbial community. J. Bacteriol. 178, 3496–3500 (1996).

    CAS  Article  Google Scholar 

  13. 13

    Veldhuis, M. J. W. & Kraay, G. W. Cell abundance and fluorescence of picoplankton in relation to growth irradiance and nitrogen availability in the Red Sea. Neth. J. Sea. Res. 31, 135–145 (1993).

    CAS  Article  Google Scholar 

  14. 14

    Partensky, F., Blanchot, J., Lantoine, F., Neveaux, J. & Marie, D. Vertical structure of picophytoplankton at different trophic sites of the subtropical northeastern Atlantic Ocean. Deep Sea Res. 43, 1191–1213 (1996).

    CAS  Article  Google Scholar 

  15. 15

    Toledo, G. & Palenik, B. Synechococcus diversity in the California Current as seen by RNA polymerase (rpoC1) gene sequences of isolated strains. Appl. Environ. Microbiol. 63, 4298–4303 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 16

    Shimada, A., Maruyama, T. & Miyachi, S. Vertical distributions and photosynthetic action spectra of two oceanic picophytoplankters, Prochlorococcus marinus and Synechococcus sp. Mar. Biol. 127, 15–23 (1996).

    CAS  Article  Google Scholar 

  17. 17

    Urbach, E., Scanlan, D. J., Distel, D. L., Waterbury, J. B. & Chisholm, S. W. Rapid diversification of marine picophytoplankton with dissimilar light-harvesting structures inferred from sequences of Prochlorococcus and Synechococcus (Cyanobacteria). J. Mol. Evol. 46, 188–201 (1998).

    ADS  CAS  Article  Google Scholar 

  18. 18

    Partensky, F., Hoepffner, N., Li, W. K. W., Ulloa, O. & Vaulot, D. Photoacclimation of Prochlorococcus sp. (Prochlorophyta) strains isolated from the north Atlantic and the Mediterranean Sea. Plant Physiol. 101, 285–296 (1993).

    CAS  Article  Google Scholar 

  19. 19

    Scanlan, D. J., Hess, W. R., Partensky, F., Newman, J. & Vaulot, D. High degree of genetic variation in Prochlorococcus (Prochlorophyta) revealed by RFLP analysis. Eur. J. Phycol. 31, 1–9 (1996).

    Article  Google Scholar 

  20. 20

    Moore, L. R. & Chisholm, S. W. Photophysiology of the marine cyanobacterium Prochlorococcus: ecotypic differences among cultured isolates. Limnol. Oceanogr.(submitted).

  21. 21

    Waterbury, J. B., Watson, S. W., Valois, F. W. & Franks, D. G. Biological and ecological characterization of the marine unicellular cyanobacterium Synechococcus. Can. Bull. Fish. Aquat. Sci. 214, 71–120 (1986).

    Google Scholar 

  22. 22

    Olson, R. J., Chisholm, S. W., Zettler, E. R. & Armbrust, E. V. Analysis of Synechococcus pigment types in the sea using single and dual beam flow cytometry. Deep Sea Res. 35, 425–440 (1988).

    ADS  CAS  Article  Google Scholar 

  23. 23

    Gallagher, J. C. Population genetics of Skeletonema costatum (Bacillariophyceae) in Narrangansett Bay. J. Phycol. 16, 464–474 (1980).

    Article  Google Scholar 

  24. 24

    Gallagher, J. C. Physiological variation and electrophoretic banding patterns of genetically different seasonal populations of Skeletonema costatum (Bacillariophyceae). J. Phycol. 18, 148–162 (1982).

    CAS  Article  Google Scholar 

  25. 25

    Platt, T., Gallegos, C. L. & Harrison, W. G. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J. Mar. Res. 38, 687–701 (1980).

    Google Scholar 

  26. 26

    Jeffrey, S. W. & Humphrey, G. F. New spectrophotometric equations for determining chlorophyll a, b, c1and c2in higher plants, algae, and natural phytoplankton. Biochem. Physiol. Pflanz. 168, 191–194 (1975).

    Article  Google Scholar 

  27. 27

    Ausubel, F. M. et al. Short Protocols in Molecular Biology(John Wiley & Sons, New York, 1992).

    Google Scholar 

  28. 28

    Maidak, B. L. et al. The RDP (Ribosomal Database Project). Nucleic Acids Res. 25, 109–111 (1997).

    CAS  Article  Google Scholar 

  29. 29

    Smith, S. W., Overbeek, R., Woese, C. R. & Gilbert, W. The genetic data environment: an expandable GUI for multiple sequence analysis. CABIOS 10, 671–675 (1994).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank M. Sogin for access to an automated DNA sequencer and helpful discussion; A. Shimada for the use of unpublished sequences of Prochlorococcus GP2 and SB; R.Olson and E. Zettler for cell sorting at sea; H. Hsu for technical assistance; and C. Cavanaugh, H. Sosik and S. Sathyendranath for helpful consultation. This work was supported by the US National Science Foundation and the US National Aeronautics and Space Administration.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Sallie W. Chisholm.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Moore, L., Rocap, G. & Chisholm, S. Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393, 464–467 (1998). https://doi.org/10.1038/30965

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.