Skip to main content
SpringerLink
Log in

Nitrogen-fixing cyanobacteria (free-living and diatom endosymbionts): their use in southern California stream bioassessment

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

A weight-of-evidence approach was used to examine how nutrient availability influences stream benthic algal community structure and to validate nutrient-response thresholds in assessing nutrient limitation. Data from 104 southern California streams spanning broad nutrient gradients revealed that relative abundance of N2-fixing heterocystous cyanobacteria (Nostoc, Calothrix), and diatoms (Epithemia, Rhopalodia)-containing cyanobacterial endosymbionts, decreased with increasing ambient inorganic N concentrations within the low end of the N gradient. Response thresholds for these N2 fixers were 0.075 mg l−1 NO3-N, 0.04 mg l−1 NH4-N, and an N:P ratio (by weight) of 15:1. The NO3-N threshold was independently validated by observing nitrogenase gene expression using real-time reverse transcriptase PCR. Morphometric analysis of cyanobacterial endosymbionts in Epithemia and Rhopalodia indicated that endosymbiont biovolume per diatom cell decreased with increasing NO3-N. Our findings indicate that abundance of heterocyst-containing cyanobacteria and endosymbiont-containing diatom cells are good indicators for rapid nutrient biomonitoring. Because heterocystous cyanobacteria and Epithemia/Rhopalodia were not always recorded together at N-limited sites, examining both assemblages jointly may provide a more comprehensive assessment of stream nutrient limitation than using either assemblage alone.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • APHA, 2006. Standard Methods for the Examination of Water and Wastewater, 20th ed. American Public Health Association, Washington, DC.

    Google Scholar 

  • Bhaya, D., R. Schwarz & A. R. Grossman, 2000. Molecular responses to environmental stress. In Whitton, B. A. & M. Potts (eds), Ecology of Cyanobacteria: Their Diversity in Time and Space. Kluwer Academic Publishers, Dordrecht, The Netherlands: 397–442.

    Google Scholar 

  • Borchardt, M. A., 1996. Nutrients. In Stevenson, R. J., M. L. Bothwell & R. L. Lowe (eds), Algal Ecology: Freshwater Benthic Ecosystems. Academic Press, San Diego, CA: 184–218.

    Google Scholar 

  • Bothe, H. 1982. Nitrogen Fixation. In Carr, N. G. & B. A. Whitton (eds), The Biology of Cyanobacteria. Botanical Monographs, Vol. 19. University of California Press, Los Angeles, CA, pp. 87–105.

  • Cairns, J. Jr., P. V. McCormick & B. R. Niederlehner, 1993. A proposed framework for developing indicators of ecosystem heath. Hydrobiologia 263: 1–44.

    Article  Google Scholar 

  • DeYoe, H. R., R. L. Lowe & J. L. Marks, 1992. Effects of nitrogen and phosphorus on the endosymbiont load of Rhopalodia gibba and Epithemia turgida Bacillariophyceae. Journal of Phycology 28: 773–777.

    Article  CAS  Google Scholar 

  • Fetscher, A. E., L. Busse & P. R. Ode, 2009. Standard operating procedures for collecting stream algae samples and associated physical habitat and chemical data for ambient bioassessments in California. California State Water Resources Control Board Surface Water Ambient Monitoring Program SWAMP Bioassessment SOP 002.

  • Geer, L. Y., A. Marchler-Bauer, R. C. Geer, L. Han, J. He, S. He, C. Liu, W. Shi & S. H. Bryant, 2010. The NCBI BioSystems database. Nucleic Acids Research 38 Database issue: D492-496.

  • Grimm, N. B. & S. G. Fisher, 1986. Nitrogen limitation in a sonoran desert stream. Journal of the North American Benthological Society 5: 2–15.

    Article  Google Scholar 

  • Grimm, N. B. & K. C. Petrone, 1997. Nitrogen fixation in a desert stream ecosystem. Biogeochemistry 37: 33–61.

    Article  CAS  Google Scholar 

  • He, X., W. Qi, B. Quiñones, S. McMahon, M. Cooley & R. E. Mandrell, 2011. Sensitive detection of Shiga Toxin 2 and some of its variants in environmental samples by a novel immuno-PCR assay. Applied and Environmental Microbiology 77: 3558–3564.

    Article  PubMed  CAS  Google Scholar 

  • Hill, B. H., R. J. Stevenson, Y. Pan, A. T. Herlihy, P. R. Kaufmann & C. B. Johnson, 2001. Comparison of correlations between environmental characteristics and stream diatom assemblages characterized at genus and species levels. Journal of the North American Benthological Society 20: 299–310.

    Article  Google Scholar 

  • Hill, W. R., 1996. Effects of light. In Stevenson, R. J., M. L. Bothwell & R. L. Lowe (eds), Algal Ecology: Freshwater Benthic Ecosystems. Academic Press, San Diego, CA: 121–148.

    Google Scholar 

  • Hill, W. R. & A. W. Knight, 1988. Nutrient and light limitation of algae in two northern California steams. Journal of Phycology 24: 125–132.

    Google Scholar 

  • Horne, A. J. & C. J. W. Carnmiggelt, 1975. Algal nitrogen fixation in California streams: seasonal cycles. Freshwater Biology 5: 461–470.

    Article  Google Scholar 

  • Kavanagh, S., C. Brennan, L. O’Connor, S. Moran, R. Salas, J. Lyons, J. Silke & M. Maher, 2010. Real-time PCR detection of Dinophysis species in Irish coastal waters. Marine Biotechnology 12: 534–542.

    Article  PubMed  CAS  Google Scholar 

  • Komárek, J. & K. Anagnostidis, 1989. Modern approach to the classification system of cyanophytes 4: Nostocales. Algological Studies 56: 247–345.

    Google Scholar 

  • Komárek, J., H. Kling & J. Komárková, 2003. Filamentous cyanobacteria. In Wehr, J. D. & R. G. Sheath (eds), Freshwater Algae of North America: Ecology and Classification. Academic Press, San Diego, CA: 117–191.

    Chapter  Google Scholar 

  • Lepš, J. & P. Šmilauer, 2003. Multivariate Analysis of Ecological Data using CANOCO. Cambridge University Press, Cambridge. UK.

    Google Scholar 

  • Lohman, K., J. R. Jones & C. Baysinger-Daniel, 1991. Experimental evidence for nitrogen limitation in a northern Ozark stream. Journal of the North American Benthological Society 10: 14–23.

    Article  Google Scholar 

  • Marcarelli, A. M., M. A. Baker & W. A. Wurstbaugh, 2008. Is in-stream N2 fixation and important N source for benthic communities and stream ecosystems? Journal of the North American Benthological Society 27: 186–211.

    Article  Google Scholar 

  • Martin-Jézéquel, V., M. Hilderbrand & M. A. Brzezinski, 2000. Silicon metabolism in diatoms: implications for growth. Journal of Phycology 36: 821–840.

    Article  Google Scholar 

  • Mateo, P., E. Berrendero, E. Perona, V. Loza & B. A. Whitton, 2010. Phosphatase activities of cyanobacteria as indicators of nutrient status in a Pyrenees river. Hydrobiologia 652: 255–268.

    Article  CAS  Google Scholar 

  • Nakayama, T., Y. Ikegami, T. Nakayama, K. Ishida, Y. Inagaki & I. Inouye, 2011. Spheroid bodies in rhopalodiacean diatoms were derived from a single endosymbiotic cyanobacterium. Journal of Plant Research 124: 93–97.

    Article  PubMed  Google Scholar 

  • Paerl, H. W., 1990. Physiological ecology and regulation of N2 fixation in natural waters. Advances in Microbial Ecology 11: 305–344.

    Article  CAS  Google Scholar 

  • Philips, E. J., J. Ihnat & M. Conroy, 1992. Nitrogen fixation by the benthic freshwater cyanobacterium Lyngbya wollei. Hydrobiologia 234: 59–64.

    Article  CAS  Google Scholar 

  • Porter, S. D., D. K. Mueller, N. E. Spahr, M. D. Munn & N. M. Dubrovsky, 2008. Efficacy of algal metrics for assessing nutrient and organic enrichment in flowing waters. Freshwater Biology 53: 1036–1054.

    Article  Google Scholar 

  • Potapova, M. G. & D. F. Charles, 2005. Choice of substrate in algae-based water-quality assessment. Journal of the North American Benthological Society 24: 415–427.

    Article  Google Scholar 

  • Prechtl, J., C. Kneip, P. Lockhart, K. Wenderoth & U.-G. Maier, 2004. Intracellular sphaeroid bodies of Rhopalodia gibba have nitrogen fixing apparatus of cyanobacterial origin. Molecular Biology and Evolution 21: 1477–1481.

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team, 2008. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

    Google Scholar 

  • Reavie, E. D., A. R. Kireta, J. C. Kingston, G. V. Sgro, N. P. Danz, R. P. Axler & T. P. Hollenhorst, 2008. Comparison of simple and multimetric diatom-based indices for Great Lakes coastline disturbance. Journal of Phycology 44: 787–802.

    Article  CAS  Google Scholar 

  • Redfield, A. C., 1958. The biological control of chemical factors in the environment. American Scientist 46: 205–221.

    CAS  Google Scholar 

  • Reir, S. T. & R. J. Stevenson, 2006. Response of periphytic algae to gradients in nitrogen and phosphorus in streamside mesocosms. Hydrobiologia 561: 131–147.

    Article  Google Scholar 

  • Rhee, G.-Y., 1974. Phosphate uptake under nitrate limitation by Scenedesmus and its ecological implication. Journal of Phycology 10: 470–475.

    CAS  Google Scholar 

  • Rozen, S. & H. Skaletsky, 2000. Primer3 on the WWW for general users and for biologist programmers. In Krawetz, S. & S. Misener (eds), Bioinformatics Methods and Protocols: Methods in Molecular Biology. Humana Press, Totowa, NJ: 365–386.

    Google Scholar 

  • Schneider, S. & E.-A. Lindstrøm, 2011. The periphyton index of trophic status PIT: a new eutrophication metric based on non-diatomaceous benthic algae in Nordic rivers. Hydrobiologia 665: 143–155.

    Article  CAS  Google Scholar 

  • Sheath, R. G. & K. M. Cole, 1992. Biogeography of stream macroalgae in North America. Journal of Phycology 28: 448–460.

    Article  Google Scholar 

  • Smith, V. H., G. D. Tilman & J. C. Nekola, 1999. Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environmental Pollution 100: 179–196.

    Article  PubMed  CAS  Google Scholar 

  • Stancheva, R., A. E. Fetscher & R. G. Sheath, 2012. A novel quantification method for stream-inhabiting, non-diatom benthic algae, and its application in bioassessment. Hydrobiologia 684: 225–239.

    Article  CAS  Google Scholar 

  • Stevenson, R. J., Y. Pan, K. M. Manoylov, C. A. Parker, D. P. Larsen & A. T. Herlihy, 2008. Development of diatom indicators of ecological conditions for streams of the western US. Journal of the North American Benthological Society 27: 1000–1016.

    Article  Google Scholar 

  • Stevenson, R. J., Y. Pan & H. van Dam, 2010. Assessing environmental conditions in rivers and streams with diatoms. In Smol, J. P. & E. F. Stoermer (eds), The Diatoms: Applications for the Environmental and Earth Sciences, 2nd ed. Cambridge University Press, Cambridge, MA: 57–85.

    Chapter  Google Scholar 

  • Stevenson, R. J., B. J. Bennett, D. N. Jordan & R. D. French, 2012. Phosphorus regulates stream injury by filamentous green algae, DO, and pH with threshold in responses. Hydrobiologia 695: 25–42.

    Article  CAS  Google Scholar 

  • Strommer, J., R. Gregerson & M. Vayda, 1993. Isolation and characterization of plant mRNA. In Glick, B. R. & J. E. Thompson (eds), Methods in Plant Molecular Biology and Biotechnology. CRC Press, Boca Raton, USA: 49–66.

    Google Scholar 

  • ter Braak, C. J. F. & C. Looman, 1995. Regression. In Jongman, R., C. ter Braak & O. van Tongeren (eds), Data Analysis in Community and Landscape Ecology. Cambridge University Press, Cambridge, UK: 29–77.

    Chapter  Google Scholar 

  • ter Braak, C. J. F. & P. Smilauer, 1998. CANOCO for Windows: Software for Canonical Community Ordination version 4. Microcomputer power, Ithaca, New York.

    Google Scholar 

  • Van Der Werff, A., 1955. A new method of concentrating and cleaning diatoms and other organisms. Proceedings of the International Association of Theoretical and Applied Limnology 12: 276–277.

    Google Scholar 

  • Whitton, B. A. & P. Mateo, 2012. Rivulariaceae. In Whitton, B. A. (ed.), Ecology of Cyanobacteria II. Their Diversity in Space and Time. Springer, London: 561–591.

    Chapter  Google Scholar 

  • Yelloly, J. M. & B. A. Whitton, 1996. Seasonal changes in ambient phosphate and phosphatase activities of the cyanobacterium Rivularia atra in intertidal pools at Tyne Sands, Scotland. Hydrobiologia 325: 201–212.

    Article  CAS  Google Scholar 

  • Zar, J. H., 1996. Biostatistical analysis, 3rd ed. Prentice Hall, Upper Saddle River, USA.

    Google Scholar 

Download references

Acknowledgments

The authors wish to acknowledge research funding from the California State Water Resources Control Board Consolidated Grants and SWAMP Programs. We thank the following people for assistance in this project: Bérengére Laslandes, Mariska Brady, Andrew Fields, Evan Thomas, Christina Fuller, Karen McLaughlin, and Martha Sutula. We thank Lilian Busse for advice on the project and Eric Stein and Stephen Weisberg for providing valuable feedback on the manuscript. We would like to thank the associate editor, Dr. Judit Padisák, and two anonymous reviewers for feedback that improved the manuscript.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, California State University San Marcos, San Marcos, CA, 92096, USA

    Rosalina Stancheva, Robert G. Sheath, Betsy A. Read, Kimberly D. McArthur & Chrystal Schroepfer

  2. University of Colorado Museum, University of Colorado Boulder, Boulder, CO, 80310, USA

    J. Patrick Kociolek

  3. Department of Biology, Southern California Coastal Water Research Project, Costa Mesa, CA, 92626, USA

    A. Elizabeth Fetscher

Authors
  1. Rosalina Stancheva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert G. Sheath
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Betsy A. Read
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kimberly D. McArthur
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chrystal Schroepfer
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. Patrick Kociolek
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. Elizabeth Fetscher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rosalina Stancheva.

Additional information

Handling editor: Judit Padisak

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stancheva, R., Sheath, R.G., Read, B.A. et al. Nitrogen-fixing cyanobacteria (free-living and diatom endosymbionts): their use in southern California stream bioassessment. Hydrobiologia 720, 111–127 (2013). https://doi.org/10.1007/s10750-013-1630-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-013-1630-6

Keywords

Search

Navigation