Fueling research on Chlamydomonas

During the past decade basic research on unicellular microalgae, including Chlamydomonas reinhardtii (commonly referred to as Chlamydomonas), has benefitted from a surge of funding addressing the need for sustainable, domestic production of high energy compounds and high-value co-products. In 2008, The Plant Journal Special Issue on ‘Harnessing Plant Biomass….’ included an article on the sustainable production of biofuels from microalgal triacylglycerols (Hu et al., 2008) that has become one of the Journal's most highly cited articles of all time, providing one measure of the increased interest in microalgae. While the commercialization of algal feed stocks for biofuel production is still in its infancy, a large number of papers focusing on the metabolism of Chlamydomonas and its changes in response to different stresses have been published. As a result, our knowledge of the biology of Chlamydomonas has increased vastly in a relatively short period of time. Thus, a Special Issue on Chlamydomonas published in The Plant Journal providing an overview of this progress seems timely. In my own research during the past decade, I expanded my scientific horizon, driven by changing federal funding priorities/opportunities and advances in genomic technology, to include not only Arabidopsis, but also Chlamydomonas and other plants and algae as new photosynthetic reference species. One lesson I took away as we started to look closer into the biology of Chlamydomonas is that the knowledge we gained in the model plant Arabidopsis cannot necessarily be transferred verbatim to Chlamydomonas or other photosynthetic eukaryotes. I certainly find this to be true in my area of expertise for certain aspects of photosynthesis and lipid metabolisms, but it is not limited to these areas of research as documented in the articles of this Special Issue. It seems apparent that exploring and capturing the biological diversity in distantly related species of photosynthetic eukaryotes will ultimately allow us to gain a deeper overall understanding of the mechanistic principles of the biological conversion of sun light into chemical energy that drive life on earth and supply our foods and fuels. Thus, The Plant Journal is adapting to the increasing spectrum of photosynthetic reference organisms studied by the community, which is reflected in the dedication of an entire Special Issue to a non-plant reference model, an alga. Historically, Chlamydomonas has been used as a genetically tractable model to study photosynthesis. Common laboratory strains can be grown heterotrophically on acetate-containing medium, as discovered in Paul Lewin's lab, allowing the isolation of mutants disrupted in photosynthesis. In a historic perspective introducing this Special Issue, Ursula Goodenough reminisces about the early days of Chlamydomonas research in the Lewin lab (Goodenough, 2015). Chlamydomonas as a biflagellate cell has also been invaluable for structure/function studies of eukaryotic flagella, and much of what is known today about these organelles in eukaryotes is based on research with Chlamydomonas. Much of this work has traditionally not been published in The Plant Journal and we were unable to solicit an article summarizing progress in research on flagella. However, The Plant Journal is open to receiving submissions of papers covering this important area of basic cell biological research. Another area of cell biology for which Chlamydomonas provides an excellent tractable experimental system is the cell cycle and its regulation based on cell size in this alga. Unlike baker's yeast, Chlamydomonas utilizes an ortholog of the mammalian Retinoblastoma suppressor protein for regulation of the cell cycle, suggesting that discoveries in Chlamydomonas cell cycle control are directly relevant to our general understanding of cell cycle control and its medically important aberrations in mammals. Cross and Umen provide details and an in-depth summary of recent progress on the analysis of the cell cycle in Chlamydomonas (Cross and Umen, 2015). Advances in research on Chlamydomonas are in part based on technological developments. The Plant Journal regularly publishes Technical Advances focused on Chlamydomonas with recent examples addressing targeted inactivation of genes with artificial miRNAs, a new set of optimized fluorescent marker proteins, and new markers and methods for mutant isolation (Rasala et al., 2013; Hu et al., 2014; Young and Purton, 2014; Terashima et al., 2015). Jonikas and Jinkerson summarize in this Special Issue the latest progress in developing molecular techniques to interrogate and edit the nuclear genome (Jinkerson and Jonikas, 2015). Because photosynthesis and primary carbon metabolism are central to the productivity of microalgae, research on these and related topics has been intensive. To adequately capture progress in this area of Chlamydomonas research, several articles in this Special Issue cover different aspects of energy and carbon metabolism. Minagawa and Tokutsu start out by summarizing progress in our current understanding of photosynthetic electron transport and its dynamic regulation in response to changing conditions (Minegawa and Tokutsu, 2015). Microalgae live in an aqueous environment where the supply of CO2 is often limiting to photoautotrophic growth. Algae such as Chlamydomonas have developed sophisticated carbon concentration mechanisms to overcome this limitation. Impressive progress has been made in understanding and describing algal carbon concentration mechanisms as summarized by Wang and colleagues (Wang et al., 2015). While light is necessary for photosynthesis, too much light is dangerous for the photosynthetic apparatus. Chlamydomonas has been fundamental in our understanding of light protective mechanisms as described by Erickson and coworkers (Erickson et al., 2015). High incidence of light is often accompanied by a drastic increase in water temperature. Adaptations to heat stress in Chlamydomonas are described by Schroda and his colleagues (cite Schroda article). Depending on the Earth's latitude, algae spend varying times of their life in the dark at night, and as photosynthetic organisms they have to switch to heterotrophic metabolism during this period. Yang and colleagues focus in their article on the ‘Life of Chlamydomonas after dark’ (Yang et al., 2015). One of the major ‘sought after’ metabolic endproducts of photosynthesis in Chlamydomonas are triacylglycerol lipids as feed stocks for biofuels. Their synthesis is intimately intertwined with general fatty acid biosynthesis and acyl-lipid metabolism. Thus, the biosynthesis of acyl-lipids and its regulation have been intensively studied during recent years, as summarized by Li-Beisson and her colleagues (Li-Beisson et al., 2015). Chlamydomonas serves not only as a basic research reference model for more biotechnologically relevant green algae, but has been directly engineered to maximize biofuel production or to produce novel bioproducts. Scranton and colleagues discuss the recent contributions of Chlamydomonas research towards fulfillment of the promise of sustainable algal biofuels and bioproducts (Scranton et al., 2015). Taking the next step towards the more efficient engineering of microalgae will be the application of synthetic biology approaches to Chlamydomonas as a ‘chassis’. Progress in genome analysis, editing, and DNA synthesis have made it possible to apply synthetic biology approaches towards the engineering of microalgae as summarized by Scaife and colleagues (Scaife et al., 2015). Biotechnological applications and the promise of sustainable production of biofuels and bioproducts from algae have been motivating factors benefitting basic research on microalgae, especially Chlamydomonas. Many of the most exciting novel insights have been basic in nature and have contributed not only to our increased understanding of mechanisms of algal growth and primary metabolism in the light but also in the dark, as reflected in this Special Issue. Discoveries involving Chlamydomonas will allow us to answer important questions of general interest for example, how metabolic/nutritional status of the cell affects cell division. Chlamydomonas may prove to be a highly tractable unicellular model to address this and other fundamental questions equal in importance to other current models. Thus, while funding for applied algal biofuel research may have struck a temporary impasse, basic research prospects focusing on Chlamydomonas have never been more outstanding. As in the past, The Plant Journal is looking forward to publishing articles describing novel basic mechanistic discoveries, technological advances or the development of community resources for microalgae research in the future.