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Glen Wheeler

MBA Senior Research Fellow
Email: glw@mba.ac.uk
Telephone: 01752 633275

Algal signalling and physiology

We are interested in the cellular mechanisms in marine phytoplankton that underpin and drive global biogeochemical cycles. We study the mechanisms algae use to respond to their environment and use algae as model organisms to study fundamental signalling processes in eukaryotes.

 

Tweiss2

 

Current research projects

Molecular mechanisms of calcification in coccolithophores

Molecular mechanisms of calcifciationCoccolithophores are abundant bloom-forming phytoplankton that play an important role in the global carbon cycle due to their ability to produce calcium carbonate plates, known as coccoliths. Changes in the chemistry of our oceans caused by increased atmospheric CO2 may have a significant impact on coccolithophore calcification. In order to help predict how coccolithophores will respond to these rapid changes in their environment, we are examining how calcification is regulated at the cellular level. We are using genomic and physiological techniques in coccolithophores to determine the cellular mechanisms responsible for calcification and how these mechanisms may respond to environmental change.

The intracellular precipitation of calcite in coccolithophores produces equimolar quanitities of H+, necessitating mechanisms for rapid H+ efflux. We have identified that coccolithophores possess a voltage-gated H+ channel in their plasma membrane which plays an important role in pH homeostasis (Taylor et al, 2011). This mechanism is highly sensitive to changes in the transmembrane H+ gradient, suggesting it may play an important role in the response of these phytoplankton to the predicted future changes in ocean pH.

 

Calcium signalling in cilia and flagella

Ca2+ signalling in cilia and flagellaCell biologists are becoming increasingly aware that cilia and flagella are important sensory organelles, which detect changes in the extracellular environment and convey these signals to the cell body. The biflagellate green alga, Chlamydomonas, is a model organism for the study of flagella function and has allowed researchers to link ciliary dysfunction to a range of human genetic disorders. We are using molecular, biochemical and cell physiological techniques to study signalling processes in Chlamydomonas flagella. We have developed techniques to image Ca2+ in both the cytosol and the flagella of Chlamydomonas and have recently demonstrated that intraflagellar Ca2+ elevations regulate the important process of intraflagellar transport (IFT) (Collingridge et al, 2013).

 

The evolution of ion channels

PhaeodactylumGFP2Eukaryote algae represent many diverse phylogenetic groups and therefore contain a wealth of genomic information relating to the evolution of fundamental cellular processes. Many ion channels associated with animal signalling processes are also present in the genomes of unicellular photosynthetic algae, including the voltage-gated Ca2+ channels, TRP channels and inositol triphosphate receptors (Wheeler and Brownlee, 2008). We are using comparative genomic approaches in combination with physiological studies to understand the evolutionary origins of these ion channels and their roles in algae.

 

The evolution of algal metabolism

Algae represent many diverse photosynthetic eukaryotes with a complex evolutionary history. These lineages became photosynthetic when they engulfed a photosynthetic cyanbacterium or algal symbiont. This has resulted in a complex heritage of their genetic material and this complexity is also reflected in their physiology. We are interested in the processes and environmental pressures that have shaped algal evolution, as this will help us understand more about algae that are alive today.

Our early work demonstrated the pathway through which vitamin C is made in plants (Wheeler et al 1998). Plants and animals use different pathways to make vitamin C and a third pathway is found in the alga, Euglena. Our recent work has examined why these different pathways exist and identified a common trend. A number of animals (including primates, guinea pigs and some bats) have lost the ability to make vitamin C due to a defect in the final enzyme in the pathway (L-gulonolactone oxidase or GULO). Our research identified that plastid acquisition in plants and algae is also linked to the loss of GULO (Wheeler et al 2015). Plants and algae replaced GULO with an alternative enzyme, which may have helped to protect them from damaging reactive oxygen derived from the chloroplast.

Many important marine algae require vitamin B12 for growth. Eukaryotes cannot Signalling between algae and bacteriasynthesise vitamin B12
and this co-factor must therefore be obtained from bacterial sources. However, only 50% of algal species require B
12 and it appears B12 dependence has arisen independently in many different lineages
throughout evolution. In collaboration with Prof Alison Smith (University of Cambridge), we are examining the cellular mechanisms responsible and the nature of the interaction between algae and bacteria. We have discovered that several algae species have recently lost the B
12-independent isoform of methionine synthase leading to dependence on exogenous sources vitamin B12 (Helliwell et al, 2011).

 

Publications:

  • Wheeler G, Ishikawa T, Pornsaksit V, Smirnoff N. (2015). Evolution of alternative biosynthetic pathways for vitamin C following plastid acquisition in photosynthetic eukaryotes. eLife. (in press).
  • Flynn KJ, Clark DR, Mitra A, Fabian H, Hansen PJ, Glibert PM, Wheeler GL, Stoecker DK, Blackford JC, Brownlee C. (2015). Ocean acidification with (de)eutrophication will alter future phytoplankton growth and succession. Proc Biol Sci. (in press).
  • Helliwell K. E., Collins S. Kazamia E. Purton S. Wheeler G. L. and Smith A.G. (2014). Fundamental shift in vitamin B12 eco-physiology of a model alga demonstrated by experimental evolution. The ISME Journal. (in press).
  • Keeling PJ, Burki F, Wilcox HM, Allam B, Allen EE, …Wheeler G… et al. (2014) The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the Functional Diversity of Eukaryotic Life in the Oceans through Transcriptome Sequencing. PLoS Biology 12(6): e1001889
  • Collingridge P, Brownlee C, Wheeler GL. (2013) Compartmentalised calcium signalling in cilia regulates intraflagellar transport. Current Biology 23(22):2311-8
  • Read BA, Kegel J, Klute MJ, Kuo A, Lefebvre SC, Maumus F, Mayer C, Miller J, Monier A, Salamov A, Young J, Aguilar M, Claverie JM, Frickenhaus S, Gonzalez K, Herman EK, Lin YC, Napier J, Ogata H, Sarno AF, Shmutz J, Schroeder D, de Vargas C, Verret F, von Dassow P, Valentin K, Van de Peer Y, Wheeler G; Emiliania huxleyi Annotation Consortium, Dacks JB, Delwiche CF, Dyhrman ST, Glöckner G, John U, Richards T, Worden AZ, Zhang X, Grigoriev IV. (2013) Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature. 499(7457), 209-13.
  • Helliwell KE, Wheeler GL, Smith AG. (2013) Widespread decay of vitamin-related pathways: coincidence or consequence?  Trends Genetics. 29(8):469-78.
  • Bach LT, Mackinder L, Schulz K, Wheeler GL, Schroeder DC, Brownlee C, Riebesell U. (2013) Dissecting the impact of CO2 and pH on the mechanisms of photosynthesis and calcification in the coccolithophore Emiliania huxleyiNew Phytologist. 199(1):121-34.
  • Flynn KJ, Blackford JC, Baird ME, Raven JA, Clark DR, Beardall J, Brownlee C, Fabian H, Wheeler GL. (2012) Changes in pH at the exterior surface of plankton with ocean acidification. Nature Climate Change. 2, 510-513
  • Chan CX, Zäuner S, Wheeler G, Grossman AR, Prochnik SE, Blouin NA, Zhuang Y, Benning C, Berg GM, Yarish C, Eriksen RL, Klein AS, Lin S, Levine I, Brawley SH, Bhattacharya D (2012). Analysis of Porphyra membrane transporters demonstrates gene transfer among photosynthetic eukaryotes and numerous sodium-coupled transport systems. Plant Physiol. 158(4):2001-12.
  • Taylor AR, Brownlee C, Wheeler GL. (2012). Proton channels in algae: reasons to be excited. Trends Plant Sci. 17(11):675-84.
  • Crawfurd KJ, Raven J, Wheeler GL, Baxter E, Joint I (2011). The response of Thalassiosira pseudonana to long-term exposure to increased CO2 and decreased pH. PLOS One. 6(10):e26695
  • Mackinder L, Wheeler GL, Schroeder DS, Von Dassow P, Riebesell U, Brownlee C. (2013) Expression of biomineralisation related ion transport genes in Emiliania huxleyi. Env Microbiol. 13(12):3250-65.
  • Helliwell KE, Wheeler GL, Leptos KC, Goldstein RE and Smith AG. (2011) Insights into the Evolution of Vitamin B12 Auxotrophy from Sequenced Algal Genomes. Mol Biol Evol. 28(10):2921-33.
  • *Taylor AR, *Chrachri A, *Wheeler GL, Goddard H and Brownlee C. A voltage-gated H+ channel underlying pH homeostasis in calcifying coccolithophores. PLOS Biology. 2011. 9(6):e1001085. (* denotes equal contribution).
  • Verret F, Taylor A, Wheeler G, Farnham G, Brownlee C. Calcium channels and their implications for evolution of calcium-based signalling in photosynthetic eukaryotes. New Phytologist. 2010. 187(1), 23-43.
  • Mackinder L, Wheeler G, Schroeder D, Riebesell U, Brownlee C. Molecular mechanisms underlying calcification in coccolithophores. Geomicrobiology. 2010. 27, 585-595.
  • Qudeimat E, Faltusz AM, Wheeler G, Lang D, Brownlee C, Reski R, Frank W. A PIIB-type Ca2+-ATPase is essential for stress adaptation in Physcomitrella patens. PNAS. 2008. 105(49) 19554-19559.
  • Wheeler GL, Brownlee C. Ca2+ signalling in plants and green algae – changing channels. Trends Plant Sci. 2008. 13(9):506-14
  • Wheeler GL, Miranda-Saavedra D, Barton GJ. Genome Analysis of the Unicellular Green Alga Chlamydomonas reinhardtii Indicates an Ancient Evolutionary Origin for Key Pattern Recognition and Cell-Signaling Protein Families. Genetics. 2008. 179(1):193-7.
  • Wheeler GL, Joint I, Brownlee C. Rapid spatiotemporal patterning of cytosolic Ca2+ underlies flagellar excision in Chlamydomonas reinhardtii. Plant J. 2008. 53(3):401-13.
  • Thompson SE, Callow JA, Callow ME, Wheeler GL, Taylor AR, Brownlee C. Membrane recycling and calcium dynamics during settlement and adhesion of zoospores of the green alga Ulva linza. Plant Cell Environ. 2007. 30(6):733-44.
  • Joint I, Tait K, Wheeler G. Cross-kingdom signalling: exploitation of bacterial quorum sensing molecules by the green seaweed Ulva. Phil Trans R Soc B. 2007. 362(1483):1223-33.
  • Conklin PL, Gatzek S, Wheeler GL, Dowdle J, Raymond MJ, Rolinski S, Isupov M, Littlechild JA, Smirnoff N. Arabidopsis thaliana VTC4 encodes L-galactose-1-P phosphatase, a plant ascorbic acid biosynthetic enzyme. J Biol Chem. 2006. 281(23):15662-70.
  • Bothwell JHF, Brownlee C, Hetherington AM, Ng CK, Wheeler GL, McAinsh MR. Biolistic delivery of Ca2+ dyes into plant and algal cells. Plant J. 2006. 46(2):327-35.
  • Wheeler GL, Tait K, Taylor A, Brownlee C, Joint I. Acyl-homoserine lactones modulate the settlement rate of zoospores of the marine alga Ulva intestinalis via a novel chemokinetic mechanism. Plant Cell Env. 2006. 29(4):608-18.
  • Wheeler GL, Grant CM. Regulation of redox homeostasis in the yeast Saccharomyces cerevisiae. Physiol. Plant. 2004 120(1):12-20.
  • Wheeler GL, Trotter EW, Dawes IW, Grant CM. Coupling of the transcriptional regulation of glutathione biosynthesis to the availability of glutathione and methionine via the Met4 and Yap1 transcription factors. J Biol Chem. 2003 278(50):49920-8.
  • Wheeler GL, Quinn KA, Perrone G, Dawes IW, Grant CM. Glutathione regulates the expression of gamma-glutamylcysteine synthetase via the Met4 transcription factor. Mol Microbiol. 2002. 46(2):545-56.
  • Collinson EJ, Wheeler GL, Garrido EO, Avery AM, Avery SV, Grant CM. The yeast glutaredoxins are active as glutathione peroxidases. J Biol Chem 2002. 277(19):16712-7.
  • Gatzek S, Wheeler GL, Smirnoff N. Antisense suppression of L-galactose dehydrogenase in Arabidopsis thaliana provides evidence for its role in ascorbate synthesis and reveals light modulated L-galactose synthesis. 2002. Plant J. 30(5):541-53.
  • Smirnoff N and Wheeler GL. Ascorbic acid in plants: biosynthesis and function. Crit Rev Biochem Mol Biol 2000. 35(4):291-314
  • Conklin PL, Norris SR, Wheeler GL, Williams EH, Smirnoff N and Last RL. Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis. PNAS 1999. 96:4198-4203
  • Wheeler GL, Jones MA and Smirnoff N. The biosynthetic pathway of vitamin C in higher plants. Nature 1998. 393:365-369

 

Book chapters:

  • Smirnoff N and Wheeler GL. Ascorbic acid metabolism in plants. In Plant Carbohydrate Biochemistry. 1999. eds JA Bryant, MM Burrell, NJ Kruger. pp 215-229, Oxford:BIOS Sci Publ.