Microbial Responses to Environmental Stressors

I have had a longstanding interest in how photosynthetic microbes sense and respond to fluctuating and multiple environmental stressors such as light and nutrients.  I have focused attentionon cyanobacteria which are important primary producers and contribute significantly to the fixed carbon budget in many terrestrial and marine environments.  Cyanobacteria have survived for ~3 billion years during periods in which there were dramatic changes in environmental conditions and they are found in extreme environments, ranging from desiccated desert crusts to high-temperature hot springs. Many cyanobacteria fix nitrogen, and release hydrogen as a by-product and are also part of harmful algal blooms worldwide.  Thus they are now being studied as organisms for the potential production of clean biofuels, as sources of fixed nitrogen and carbon and for the production of secondary metabolites. 

Early on, we studied how cyanobacteria respond to phosphorus deprivation, which led to the identification of novel phosphatases and the recognition that there is interplay between nutrient and light stress in the model organisms Synechococcus and Synechocystis. At the same time, I was also involved in the identification of small proteins (HLIPS) that are highly induced under prolonged high light or UVA stress and allow cyanobacteria to adapt to high light stress. Interestingly, these proteins turned out to be part of a large super-family of the light harvesting proteins that are conserved in all plants/algae and recently we have gone back to following these proteins as markers for high light stress acclimation in marine and thermophilic cyanobacteria. The ability of cyanobacteria to survive some of the harshest environments on the planet raises important challenges in our understanding of how phototrophs respond to stress at a mechanistic and systems level. A number of approaches including comparative genomics (over 50 cyanobacterial genomes are available..and the list keeps growing!) and the ability to carry out detailed biochemistry combined with genetics make this an exciting field for study.

We have recently focused our attention on thermophilic cyanobacteria in the microbial mats of alkaline hot springs in Yellowstone National Park (see “Microbial communities” project).  Based on a comparative genomic approach of two closely related completely sequenced isolates we chose to explore how these organisms respond to high light stress, to phosphate deprivation and their ability to fix nitrogen. Using axenic isolates we have characterized these responses in some amount of detail. We find that these organisms have a large suite of genes (part of the pho regulon) to respond to phosphorus stress. Interestingly, only one of these isolates carries genes for phosphonate utilization which allows them to grow on phosphonates as a sole P source. Other new details regarding phosphonate utilization and the regulation of related pathways have emerged from these studies.  We are continuing this research with the overarching view that it is critical to work in situ under environmentally relevant conditions as well as with isolates under defined conditions.

RELEVANT PUBLICATIONS (PDF version available under Publications)

1.    Gomez-Garcia M.R., M. Davison, M. B.-Hartnung A. R. Grossman, D Bhaya Alternative Pathways for Phosphonate Metabolism in Thermophilic Cyanobacteria from Microbial Mats ISME J. EPub July 15, 2010
2.    Jensen S., Steunou, A-S, Bhaya, D, Kühl M., Arthur R. Grossman In situ Dynamics of O2, pH and Cyanobacterial Transcripts Associated with Inorganic Carbon Concentration, Photosynthesis and Detoxification of Reactive Oxygen Species in Hot Spring Microbial Mats ISME J  Epub Aug 26, 2010
3.    Adams M, Gomez, R. Grossman A.R. and D. Bhaya Responses of thermophilic Synechococcus sp. to phosphate deprivation and growth on phosphonate. J Bacteriol. 2008 Dec; 190 (24):8171-84..
4.    Steunou A-S, Jensen S, Brecht E., Becraft E.D., Bateson, Kilian O, Bhaya D. , Ward D.M., Peters J.W., Grossman A.R., Kühl M. (2008) Regulation of nif Gene Expression and the Energetics of N2 Fixation over the Diel Cycle in a Hot Spring Microbial Mat ISME Journal, 2(4):364-78. Epub 2008 Mar 6.
5.    Kilian O, Steunou A-S., Grossman A.R., Bhaya D. A novel two domain-fusion protein in cyanobacteria with similarity to the CAB/ELIP/HLIP superfamily: Evolutionary implications and regulation (2008) Molecular Plant 1;155-166
6.    Bhaya D., Grossman, A.R., Steunou A.S., N.Khuri, F.M. Cohan, N. Hamamura, M. C. Melendrez, M. M. Bateson, D. M. Ward, J.F. Heidelberg (2007) Genomic, metagenomic and functional analyses of cyanobacteria from hot-spring microbial mats reveal an unexpected diversity in nutrient utilization strategies  ISME J: 1(8):703-13 Epub Oct, 2007
7.    Kilian O, A-S Steunou, F. Fazeli, S. Bailey, D. Bhaya, A R. Grossman: Light Responses of Thermophilic Synechococcus isolates from the Microbial Mats of Octopus Spring (2007) Appl. Environ, Microbiol. 73: 4268-4278
8.    Steunou, A.S., Bhaya, D., Bateson, M., Melendrez, M., Ward, D., Brecht, E., Peters, J.W., Kühl, K, Grossman, A.R. (2006) In situ analysis of nitrogen fixation and metabolic switching in unicellular thermophilic cyanobacteria inhabiting a hot-spring microbial mat Proc. Natl. Acad. Sci. U.S.A.103:2398-2407
9.    Mrázek, J., D. Bhaya, A. R. Grossman and S. Karlin (2001) Highly expressed and alien genes of the Synechocystis genome. Nucleic Acids Res. 29:1590-601
10.    Bhaya, D., D.Vaulot, P.Amin, A.W. Takahashi and A.R. Grossman (2000) Isolation of regulated genes of the unicellular cyanobacterium Synechocystis sp.strain PCC6803 by differential display. J. Bacteriol. 182:5692-5699.
11.    Bhaya, D., R. Schwarz and A. R. Grossman (2000)  “Molecular responses to environmental stresses” in “Ecology of Cyanobacteria: Their diversity in time and space” Ed. B.A.Whitton and M.Potts, Kluwer Academic Publishers Ltd. pp 397-442
12.    Dolganov, N., D. Bhaya and A.R. Grossman (1995) Cyanobacterial protein with homology to the chlorophyll a/b binding proteins of plants: Evolution and regulation. Proc. Natl. Acad. Sci. U.S.A., 92: 636-640
13.    Grossman. A.R., D. Bhaya and J.L. Collier (1994) Specific and general responses of cyanobacteria to macronutrient deprivation. In Cellular and Molecular Biology of Phosphate and Phosphorylated Compounds in Microorganisms. Eds. Torriani-Gorini, Yagil and Silver, ASM Press, -Washington DC, USA.  pp. 112-118