Algal signalling and physiology
Marine phytoplankton must constantly sense and respond to their dynamic environment in order to survive
We are interested in the cellular mechanisms in marine phytoplankton that underpin and drive global biogeochemical cycles.
Using a combination of genomic and physiological techniques, we study how algae sense and respond to their environment.
Much of our research uses single cell microscopy approaches to directly visualise signalling processes. Some examples are shown below.
Phytoplankton cells differ considerably in cell size. This is particularly true of the marine diatoms, which can differ in diameter from a few micrometers up to huge cells or several hundred micrometers. Cell size has a major impact on the ability of cells to acquire nutrients, with large cells surrounded by a substantial diffusion boundary layer. The microenvironment around cells, termed the ’phycosphere’, likely plays an important role in the physiology of phytoplankton and their interactions with other marine microbes.
We have been studying the effect of cell size on the uptake of carbon by marine diatoms. Marine diatoms, like all phytoplankton, operate a carbon concentrating mechanism (CCM) to overcome limitations in the diffusive supply of CO2 to the cell surface. As limitations to the supply of CO2 are greater in large cells (due to their diffusive boundary layer), these processes may directly influence the composition of diatom communities. We have recently developed ion selective microelectrodes to allow us to measure carbonate chemistry at the surface of individual diatom cells for the first time (Chrachri et al 2018). These novel approaches will allow us to address some of the major uncertainties relating to carbon acquisition in diatoms and better understand how these constraints influence diatom community composition.
Coccolithophores 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 and how these mechanisms may respond to environmental change.
We have recently made the surprising discovery that some coccolithophores require silicon in order to produce their coccoliths (Durak et al 2016). These species possess silicon transporters that are related to those found in extensively silicified phytoplankton, such as the diatoms. This finding has important implications for our understanding of the evolution of calcification and silicification by marine organisms. The absence of a requirement for silicon in bloom-forming coccolithophore species, such as Emiliania huxleyi, may have enhanced their ability to compete with the heavily silicified diatoms.
We are interested in how algae sense and respond to their environment. Signalling mechanisms allow algal cells to adjust rapidly to stressors such as light, touch or temperature and a better understanding of these processes will help us determine the ability of different algae to cope with a changing environment.
The phytoplankton found in our oceans are incredibly diverse. By studying their different signalling mechanisms we can gain insight into 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.
Surprisingly, we found a completely novel class of voltage-gated ion channels in algae, called the EukCats. We showed that the diatoms possess EukCatA channels, which play an important role in Ca2+ signalling (Helliwell et al, 2019). Coccolithophores possess another class of channels (EukCatB) that act as fast-activating Na+ channels (Helliwell et al 2020). These discoveries indicate that algae possess highly unusual cell signalling mechanisms that likely have a major impact on the way they interact with their environment.
Cell 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).
Algae represent many diverse photosynthetic eukaryotes with a complex evolutionary history. These lineages became photosynthetic when they engulfed a photosynthetic cyanobacterium 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.
Assessing how cell size constrains carbon uptake in diatoms using direct measurements of cell surface carbonate chemistry
Marine diatoms are major contributors to global primary productivity and one of the most abundant photosynthetic organisms on our planet, but much remains to be learnt about the mechanisms through which they acquire carbon from seawater. In particular, the role of the diffusive boundary layer...
Continuing Genetic Tool Development in Marine Protists to Advance Nascent Experimental Model Systems : Development of gene editing technologies within the haptophyte algae
This project aims to develop molecular genetic tools in the haptophyte algae. Strains will be selected that exhibit rapid and robust growth in laboratory culture as candidate model organism for the development of genetic tools within the haptophytes. Our approach will be to...
Coccolithophore calcification: An unexpected requirement for silicon
The role of ciliary calcium signalling in the regulation of intraflagellar transport
- Helliwell KE, Kleiner F., Hardstaff H., Chrachri A., Salmon D., Smirnoff N., Wheeler GL, and Brownlee C. (2021). Spatiotemporal patterns of intracellular Ca2+ signalling govern hypo-osmotic stress resilience in marine diatoms. New Phytologist, In press, https://doi.org/10.1111/nph.17162.
- Helliwell KE, Harrison E., Christie-Oleza J, Downe J, Rees A, Al-Moosawi L, Brownlee C., Wheeler GL. (2021) A novel Ca2+ signalling pathway co-ordinates environmental phosphorus sensing and nitrogen metabolism in marine diatoms. Current Biology, 31: 1-12, https://doi.org/10.1016/j.cub.2020.11.073.
- Helliwell KE, Chrachri A, Koester J, Wharam S, Taylor A, Wheeler GL, Brownlee C. (2020). A novel single-domain Na+-selective voltage-gated channel in photosynthetic eukaryotes. Plant Physiol. p.00889.2020.
- Meyer EM, Langer G, Brownlee C, Wheeler GL, Taylor AR (2020). Sr in coccoliths of Scyphosphaera apsteinii: Partitioning behavior and role in coccolith morphogenesis. Geochimica et Cosmochimica Acta 285, 41-54
- Brownlee C, Langer G, Wheeler GL (2020). Coccolithophore calcification: Changing paradigms in changing oceans. Acta Biomaterialia S1742-7061(20)30436-0.
- de Vries J, Monteiro F, Wheeler G, Poulton A, Godrijan J, Cerino, F, et al (2020). The haplo-diplontic life cycle expands niche space of coccolithophores. Biogeosciences Discussions, 1-39. doi.org/10.5194/bg-2020-194.
- Laundon D, Chrismas N, Wheeler GL, Cunliffe M (2020). Chytrid rhizoid morphogenesis resembles hyphal development in multicellular fungi and is adaptive to resource availability. Proc Roy Soc B 287 (1928), 20200433.
- Faktorová D, Nisbet RER, Robledo JAF, Casacuberta E, Sudek L, ..Wheeler GL…et al (2020). Genetic tool development in marine protists: Emerging model organisms for experimental cell biology. Nature Methods 17 (5), 481-494.
- McCoy SJ, Santillán‐Sarmiento A, Brown MT, Widdicombe S, Wheeler GL (2020). Photosynthetic Responses of Turf‐forming Red Macroalgae to High CO2 Conditions. J Phycol 56 (1), 85-96.
- Helliwell KE, Chrachri A, Koester J, Wharam S, Verret F, Taylor AR, Wheeler GL, and Brownlee C. (2019). Alternative mechanisms for fast Na+/Ca2+ signalling in eukaryotes via a novel class of single-domain voltage-gated channels. Current Biology. 29 (9), 1503-1511.
- Cooper MB, Kazamia E, Helliwell KE, Kudahl UJ, Sayer A, Wheeler, GL, & Smith AG. (2018). Cross-exchange of B-vitamins underpins a mutualistic interaction between Ostreococcus tauri and Dinoroseobacter shibae. ISME J. https://doi.org/10.1038/s41396-018-0274-y
- Walker CE, Heath S, Salmon DL, Smirnoff N, Langer G, Taylor AR, Brownlee C, Wheeler GL (2018). An Extracellular Polysaccharide-Rich Organic Layer Contributes to Organization of the Coccosphere in Coccolithophores. Front. Mar. Sci., doi.org/10.3389/fmars.2018.00306.
- Walker CE, Taylor AR, Langer G, Durak GM, Heath S, Probert I, Tyrrell T, Brownlee C, Wheeler GL (2018). The requirement for calcification differs between ecologically important coccolithophore species. New Phytol. doi: 10.1111/nph.15272.
- Wheeler, G; Helliwell, KE; Brownlee, C (2018). Calcium signalling in algae. Perspectives in Phycology. doi: 10.1127/pip/2018/0082.
- Chrachri A, Hopkinson BM, Flynn K, Brownlee C, Wheeler GL (2018) Dynamic changes in carbonate chemistry in the microenvironment around single marine phytoplankton cells. Nature Commun. 9:74
- Durak GM, Brownlee C, Wheeler GL. (2017) The role of the cytoskeleton in biomineralisation in haptophyte algae. Sci. Reports. 7, 15409.
- Brawley SH, Blouin NA, Ficko-Blean E, Wheeler GL, et al. (2017). Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). PNAS. 114 (31):E6361–E6370.
- Taylor AR, Brownlee C, Wheeler G (2017) Coccolithophore cell biology: chalking up progress. Ann Rev Mar Sci. 9:18.1–18.28.
- Marron AO, Ratcliffe S, Wheeler GL, Goldstein RE, King N, Not F, de Vargas C, Richter DJ. (2016). The evolution of silicon transport in eukaryotes. Mol Biol Evol. 33(12):3226-3248.
- Bickerton P, Sello S, Brownlee C, Pittman JK, Wheeler GL. (2016). Spatial and temporal specificity of Ca2+ signalling in Chlamydomonas reinhardtii in response to osmotic stress. New Phytol. 2016. doi: 10.1111/nph.14128.
- Flynn KJ, Clark DR, Wheeler G. (2016). The role of coccolithophore calcification in bioengineering their environment. Proc Biol Sci. 283(1833). pii: 20161099.
- Durak GM, Taylor AR, Walker CE, Probert I, de Vargas C, Audic S, Schroeder D, Brownlee C, Wheeler GL. (2016). A role for diatom-like silicon transporters in calcifying coccolithophores. Nature Commun. 7:10543.
- Brownlee C, Wheeler GL, Taylor AR. (2015) Coccolithophore biomineralization: New questions, new answers. Semin Cell Dev Biol. 46:11-6.
- Wheeler G, Ishikawa T, Pornsaksit V, Smirnoff N. (2015). Evolution of alternative biosynthetic pathways for vitamin C following plastid acquisition in photosynthetic eukaryotes. eLife 4:e06369.
- 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. 282(1804):20142604.
- 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. 9(6):1446-55.
- 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 huxleyi. New 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
- Calcium-Dependent Signalling Processes in Chlamydomonas (2017). Wheeler GL. Chlamydomonas: Molecular Genetics and Physiology, 233-255
Ca2+ elevations in Chlamydomonas flagella viewed by TIRF microscopy
Intraflagellar transport in Chlamydomonas during gliding motility
Cell division in a coccolithophore (Coccolithus braarudii)