Genomic imprints of unparalleled growth.
Chlorophyta
algal evolution
codon bias
growth rate
introns
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
10 Dec 2023
10 Dec 2023
Historique:
received:
29
08
2023
accepted:
31
10
2023
medline:
11
12
2023
pubmed:
11
12
2023
entrez:
10
12
2023
Statut:
aheadofprint
Résumé
Chlorella ohadii was isolated from desert biological soil crusts, one of the harshest habitats on Earth, and is emerging as an exciting new green model for studying growth, photosynthesis and metabolism under a wide range of conditions. Here, we compared the genome of C. ohadii, the fastest growing alga on record, to that of other green algae, to reveal the genomic imprints empowering its unparalleled growth rate and resistance to various stressors, including extreme illumination. This included the genome of its close relative, but slower growing and photodamage sensitive, C. sorokiniana UTEX 1663. A larger number of ribosome-encoding genes, high intron abundance, increased codon bias and unique genes potentially involved in metabolic flexibility and resistance to photodamage are all consistent with the faster growth of C. ohadii. Some of these characteristics highlight general trends in Chlorophyta and Chlorella spp. evolution, and others open new broad avenues for mechanistic exploration of their relationship with growth. This work entails a unique case study for the genomic adaptations and costs of exceptionally fast growth and sheds light on the genomic signatures of fast growth in photosynthetic cells. It also provides an important resource for future studies leveraging the unique properties of C. ohadii for photosynthesis and stress response research alongside their utilization for synthetic biology and biotechnology aims.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.
Références
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403-410.
Ananyev G, Gates C, Kaplan A, Dismukes GC. 2017. Photosystem II-cyclic electron flow powers exceptional photoprotection and record growth in the microalga Chlorella ohadii. Biochimica et Biophysica Acta-Bioenergetics 1858: 873-883.
Andersen T, Elser JJ, Hessen DO. 2004. Stoichiometry and population dynamics. Ecology Letters 7: 884-900.
Aro E-M, Virgin I, Andersson B. 1993. Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochimica et Biophysica Acta 1143: 113-134.
Arriola MB, Velmurugan N, Zhang Y, Plunkett MH, Hondzo H, Barney BM. 2018. Genome sequences of Chlorella sorokiniana UTEX 1602 and Micractinium conductrix SAG 241.80: implications to maltose excretion by a green alga. The Plant Journal 93: 566-586.
Back G, Walther D. 2021. Identification of cis-regulatory motifs in first introns and the prediction of intron-mediated enhancement of gene expression in Arabidopsis thaliana. BMC Genomics 22: 390.
Baier T, Jacobebbinghaus N, Einhaus A, Lauersen KJ, Kruse O. 2020. Introns mediate post-transcriptional enhancement of nuclear gene expression in the green microalga Chlamydomonas reinhardtii. PLoS Genetics 16: e1008944.
Baier T, Wichmann J, Kruse O, Lauersen KJ. 2018. Intron-containing algal transgenes mediate efficient recombinant gene expression in the green microalga Chlamydomonas reinhardtii. Nucleic Acids Research 46: 6909-6919.
Bailey S, Grossman A. 2008. Photoprotection in Cyanobacteria: regulation of light harvesting. Photochemistry and Photobiology 84: 1410-1420.
Banse K. 1976. Rates of growth, respiration and photosynthesis of unicellular algae as related to cell size - a review. Journal of Phycology 12: 135-140.
Baroli I, Gutman BL, Ledford HK, Shin JW, Chin BL, Havaux M, Niyogi KK. 2004. Photo-oxidative stress in a xanthophyll-deficient mutant of Chlamydomonas. The Journal of Biological Chemistry 279: 6337-6344.
Beardall J, Allen D, Bragg J, Finkel ZV, Flynn KJ, Quigg A, Rees T, Alwyn V, Richardson A, Raven JA. 2009. Allometry and stoichiometry of unicellular, colonial and multicellular phytoplankton. New Phytologist 181: 295-309.
Blanc G, Duncan G, Agarkova I, Borodovsky M, Gurnon J, Kuo A, Lindquist E, Lucas S, Pangilinan J, Polle J et al. 2010. The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell 22: 2943-2955.
Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114-2120.
Bonnet A, Grosso AR, Elkaoutari A, Coleno E, Presle A, Sridhara SC, Janbon G, Géli V, De Almeida SF, Palancade B. 2017. Introns protect eukaryotic genomes from transcription-associated genetic instability. Molecular Cell 67: 608-621.
Borisa AC, Bhatt HG. 2017. A comprehensive review on Aurora kinase: small molecule inhibitors and clinical trial studies. European Journal of Medicinal Chemistry 140: 1-19.
Bowler C, DE Martino A, Falciatore A. 2010. Diatom cell division in an environmental context. Current Opinion in Plant Biology 13: 623-630.
Brock TD. 1978. Thermophilic microorganisms and life at high temperatures. New York, NY, USA: Springer-Verlag.
Burnap RL. 2015. Systems and photosystems: cellular limits of autotrophic productivity in Cyanobacteria. Frontiers in Bioengineering and Biotechnology 3: 1.
Campbell D, Clarke AK, Gustafsson P, Oquist G. 1996. D1 exchange and the Photosystem II repair cycle in the cyanobacterium Synechococcus. Plant Science 115: 183-190.
Cardona T, Sedoud A, Cox N, Rutherford AW. 2012. Charge separation in Photosystem II: a comparative and evolutionary overview. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1817: 26-43.
Caspy I, Neumann E, Fadeeva M, Liveanu V, Savitsky A, Frank A, Kalisman YL, Shkolnisky Y, Murik O, Treves H et al. 2021. Cryo-EM photosystem I structure reveals adaptation mechanisms to extreme high light in Chlorella ohadii. Nature Plants 7: 1314-1322.
Cecchin M, Marcolungo L, Rossato M, Girolomoni L, Cosentino E, Cuine S, Li-Beisson Y, Delledonne M, Ballottari M. 2019. Chlorella vulgaris genome assembly and annotation reveals the molecular basis for metabolic acclimation to high light conditions. The Plant Journal 100: 1289-1305.
Chen K, Guo T, Li X-M, Yang Y-B, Dong N-Q, Shi C-L, Ye W-W, Shan J-X, Lin H-X. 2019. NAL8 encodes a prohibitin that contributes to leaf and spikelet development by regulating mitochondria and chloroplasts stability in rice. BMC Plant Biology 19: 395.
Cheng Y-S, Labavitch J, Vandergheynst JS. 2015. Organic and inorganic nitrogen impact Chlorella variabilis productivity and host quality for viral production and cell lysis. Applied Biochemistry and Biotechnology 176: 467-479.
Cheng Z, Mugler CF, Keskin A, Hodapp S, Chan LY, Weis K, Mertins P, Regev A, Jovanovic M, Brar GA. 2019. Small and large ribosomal subunit deficiencies lead to distinct gene expression signatures that reflect cellular growth rate. Molecular Cell 73: 36-47.
Chowdhary AK, Kishi M, Toda T. 2022. Enhanced growth of Chromochloris zofingiensis through the transition of nutritional modes. Algal Research 65: 102723.
Couradeau E, Karaoz U, Lim HC, Nunes DA Rocha U, Northen T, Brodie E, Garcia-Pichel F. 2016. Bacteria increase arid-land soil surface temperature through the production of sunscreens. Nature Communications 7: 10373.
Croce R, Van Grondelle R, Van Amerongen H, Van Stokkum I. 2018. Light harvesting in photosynthesis. Boca Raton, FL, USA: CRC Press.
Dadras A, Fürst-Jansen JMR, Darienko T, Krone D, Scholz P, Sun S, Herrfurth C, Rieseberg TP, Irisarri I, Steinkamp R et al. 2023. Environmental gradients reveal stress hubs pre-dating plant terrestrialization. Nature Plants 9: 1419-1438.
Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T. 2020. ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Molecular Biology and Evolution 37: 291-294.
De Vries J, Rensing SA. 2020. Gene gains paved the path to land. Nature Plants 6: 7-8.
De-Bashan LE, Trejo A, Huss VAR, Hernandez JP, Bashan Y. 2008. Chlorella sorokiniana UTEX 2805, a heat and intense, sunlight-tolerant microalga with potential for removing ammonium from wastewater. Bioresource Technology 99: 4980-4989.
Dönz O. 1934. Chlorella zofingiensis, eine neue Bodenalge. Berichte der Deutschen Botanischen Gesellschaft 43: 127-131.
Duan J, Shi J, Ge X, Dölken L, Moy W, He D, Shi S, Sanders AR, Ross J, Gejman PV. 2013. Genome-wide survey of interindividual differences of RNA stability in human lymphoblastoid cell lines. Scientific Reports 3: 1318.
Emanuelsson O, Brunak S, Von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2: 953-971.
Emanuelsson O, Nielsen H, Von Heijne G. 1999. ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Science 8: 978-984.
Emms DM, Kelly S. 2019. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biology 20: 238.
Erickson E, Wakao S, Niyogi KK. 2015. Light stress and photoprotection in Chlamydomonas reinhardtii. The Plant Journal 82: 449-465.
Fanesi A, Raven JA, Giordano M. 2014. Growth rate affects the responses of the green alga Tetraselmis suecica to external perturbations. Plant, Cell & Environment 37: 512-519.
Feng X, Zheng J, Irisarri I, Yu H, Zheng B, Ali Z, De Vries S, Keller J, Fürst-Jansen JMR, Dadras A et al. 2023. Chromosome-level genomes of multicellular algal sisters to land plants illuminate signaling network evolution. bioRxiv. doi: 10.1101/2023.01.31.526407.
Fernandez-Pozo N, Bombarely A. 2022. EasyGDB: a low-maintenance and highly customizable system to develop genomics portals. Bioinformatics 38: 4048-4050.
Finazzi G, Johnson GN, DALL'osto L, Zito F, Bonente G, Bassi R, Wollman FA. 2006. Nonphotochemical quenching of chlorophyll fluorescence in Chlamydomonas reinhardtii. Biochemistry 45: 1490-1498.
Flynn KJ, Raven JA. 2017. What is the limit for photoautotrophic plankton growth rates? Journal of Plankton Research 39: 13-22.
Flynn KJ, Raven JA, Rees TAV, Finkel Z, Quigg A, Beardall J. 2010. Is the growth rate hypothesis applicable to microalgae? Journal of Phycology 46: 1-12.
Foyer CH, Ruban AV, Noctor G. 2017. Viewing oxidative stress through the lens of oxidative signalling rather than damage. Biochemical Journal 474: 877-883.
Gabilly ST, Baker CR, Wakao S, Crisanto T, Guan K, Bi K, Guiet E, Guadagno CR, Niyogi KK. 2019. Regulation of photoprotection gene expression in Chlamydomonas by a putative E3 ubiquitin ligase complex and a homolog of CONSTANS. Proceedings of the National Academy of Sciences, USA 116: 17556-17562.
Gao C, Wang Y, Shen Y, Dong Y, Xi H, Junbiao D, Qingyu W. 2014. Oil accumulation mechanisms of the oleaginous microalga Chlorella protothecoides revealed through its genome, transcriptomes, and proteomes. BMC Genomics 15: 582.
Garcia-Pichel F, Loza V, Marusenko Y, Mateo P, Potrafka Ruth M. 2013. Temperature drives the continental-scale distribution of key microbes in topsoil communities. Science 340: 1574-1577.
Gollan PJ, Lima-Melo Y, Tiwari A, Tikkanen M, Aro E-M. 2017. Interaction between photosynthetic electron transport and chloroplast sinks triggers protection and signalling important for plant productivity. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 372: 20160390.
Gorbunov MY, Kuzminov FI, Fadeev VV, Kim JD, Falkowski PG. 2011. A kinetic model of non-photochemical quenching in cyanobacteria. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1807: 1591-1599.
Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talon M, Dopazo J, Conesa A. 2008. High-throughput functional annotation and data mining with the Blast2Go suite. Nucleic Acids Research 36: 3420-3435.
Greiner S, Lehwark P, Bock R. 2019. OrganellarGenomeDRAW (OGDRAW) v.1.3.1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Research 47: W59-W64.
Guarnieri MT, Levering J, Henard CA, Boore JL, Betenbaugh MJ, Zengler K, Knoshaug EP. 2018. Genome sequence of the oleaginous green alga, Chlorella vulgaris UTEX 395. Frontiers in Bioengineering and Biotechnology 6: 37.
Guida BS, Garcia-Pichel F. 2016. Extreme cellular adaptations and cell differentiation required by a cyanobacterium for carbonate excavation. Proceedings of the National Academy of Sciences, USA 113: 5712-5717.
Gurevich A, Saveliev V, Vyahhi N, Tesler G. 2013. Quast: quality assessment tool for genome assemblies. Bioinformatics 29: 1072-1075.
Hernández-Reyes C, Lichtenberg E, Keller J, Delaux PM, Ott T, Schenk ST. 2022. NIN-like proteins: interesting players in rhizobia-induced nitrate signaling response during interaction with non-legume host Arabidopsis thaliana. Molecular Plant-Microbe Interactions 35: 230-243.
Hernando-Rodríguez B, Artal-Sanz M. 2018. Mitochondrial quality control mechanisms and the PHB (Prohibitin) complex. Cell 7: 238.
Hessen DO, Ventura M, Elser JJ. 2008. Do phosphorus requirements for RNA limit genome size in crustacean zooplankton? Genome 51: 685-691.
Hiss M, Schneider L, Grosche C, Barth MA, Neu C, Symeonidi A, Ullrich KK, Perroud P-F, Schallenberg-Rüdinger M, Rensing SA. 2017. Combination of the endogenous lhcsr1 promoter and codon usage optimization boosts protein expression in the moss Physcomitrella patens. Frontiers in Plant Science 8: 1842.
Hovde BT, Hanschen ER, Steadman Tyler CR, Lo C-C, Kunde Y, Davenport K, Daligault H, Msanne J, Canny S, Eyun S-I et al. 2018. Genomic characterization reveals significant divergence within Chlorella sorokiniana (Chlorellales, Trebouxiophyceae). Algal Research 35: 449-461.
Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ, Von Mering C, Bork P. 2017. Fast genome-wide functional annotation through orthology assignment by eggNOG-Mapper. Molecular Biology and Evolution 34: 2115-2122.
Jahns P, Holzwarth AR. 2012. The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1817: 182-193.
Juneja A, Chaplen FWR, Murthy GS. 2016. Genome scale metabolic reconstruction of Chlorella variabilis for exploring its metabolic potential for biofuels. Bioresource Technology 213: 103-110.
Kalra I, Wang X, Cvetkovska M, Jeong J, Mchargue W, Zhang R, Hüner N, Yuan JS, Morgan-Kiss R. 2020. Chlamydomonas sp. UWO 241 exhibits high cyclic electron flow and rewired metabolism under high salinity. Plant Physiology 183: 588-601.
Keren N, Krieger-Liszkay A. 2011. Photoinhibition: molecular mechanisms and physiological significance. Physiologia Plantarum 142: 1-5.
Kessler E. 1972. Physiologische und biochemische Beiträge zur Taxonomie der Gattung Chlorella. Archiv für Mikrobiologie 87: 243-248.
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology 14: R36.
Kodama Y, Fujishima M. 2015. Differences in infectivity between endosymbiotic Chlorella variabilis cultivated outside host Paramecium bursaria for 50 years and those immediately isolated from host cells after one year of reendosymbiosis. Biology Open 5: 55-61.
Koyama A, Harlow B, Kuske CR, Belnap J, Evans RD. 2018. Plant and microbial biomarkers suggest mechanisms of soil organic carbon accumulation in a Mojave Desert ecosystem under elevated CO2. Soil Biology and Biochemistry 120: 48-57.
Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. 2019. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35: 4453-4455.
Krupnik T, Kotabová E, Van Bezouwen LS, Mazur R, Garstka M, Nixon PJ, Barber J, Kaňa R, Boekema EJ, Kargul J. 2013. A reaction centre-dependent photoprotection mechanism in a highly robust photosystem II from an extremophilic red alga Cyanidioschyzon merolae. The Journal of Biological Chemistry 288: 23529-23542.
Kushner DJ. 1978. Microbial life in extreme environment. London, UK: Academic Press.
Lang D, Weiche B, Timmerhaus G, Richardt S, Riano-Pachon DM, Correa LG, Reski R, Mueller-Roeber B, Rensing SA. 2010. Genome-wide phylogenetic comparative analysis of plant transcriptional regulation: a timeline of loss, gain, expansion, and correlation with complexity. Genome Biology and Evolution 2: 488-503.
Lasin P, Weise A, Reinders A, Ward JM. 2020. Arabidopsis sucrose transporter AtSuc1 introns act as strong enhancers of expression. Plant and Cell Physiology 61: 1054-1063.
Levin BR, Mccall IC, Perrot V, Weiss H, Ovesepian A, Baquero F. 2017. A numbers game: ribosome densities, bacterial growth, and antibiotic-mediated stasis and death. mBio 8: e02253-16.
Levin G, Kulikovsky S, Liveanu V, Eichenbaum B, Meir A, Isaacson T, Tadmor Y, Adir N, Schuster G. 2021. The desert green algae Chlorella ohadii thrives at excessively high light intensities by exceptionally enhancing the mechanisms that protect photosynthesis from photoinhibition. The Plant Journal 106: 1260-1277.
Li ZR, Wakao S, Fischer BB, Niyogi KK. 2009. Sensing and responding to excess light. Annual Review of Plant Biology 60: 239-260.
Liu C, Xu X, Kan J, Cheng ZM, Chang Y, Lin J, Li H. 2020. Genome-wide analysis of the C3H zinc finger family reveals its functions in salt stress responses of Pyrus betulaefolia. PeerJ 8: e9328.
Liu Y, Wei D, Chen W. 2022. Oleaginous microalga Coccomyxa subellipsoidea as a highly effective cell factory for CO(2) fixation and high-protein biomass production by optimal supply of inorganic carbon and nitrogen. Frontiers in Bioengineering and Biotechnology 10: 921024.
Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L et al. 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245-250.
Monroe JG, Srikant T, Carbonell-Bejerano P, Becker C, Lensink M, Exposito-Alonso M, Klein M, Hildebrandt J, Neumann M, Kliebenstein D et al. 2022. Mutation bias reflects natural selection in Arabidopsis thaliana. Nature 602: 101-105.
Moody EK, Rugenski AT, Sabo JL, Turner BL, Elser JJ. 2017. Does the growth rate hypothesis apply across temperatures? Variation in the growth rate and body phosphorus of neotropical benthic grazers. Frontiers in Environmental Science 5.
Mueller TJ, Ungerer JL, Pakrasi HB, Maranas CD. 2017. Identifying the metabolic differences of a fast-growth phenotype in Synechococcus UTEX 2973. Scientific Reports 7: 41569.
Nalley JO, O'donnell DR, Litchman E. 2018. Temperature effects on growth rates and fatty acid content in freshwater algae and cyanobacteria. Algal Research 35: 500-507.
Ohad I, Berg A, Berkowicz SM, Kaplan A, Keren N. 2011. Photoinactivation of photosystem II: is there more than one way to skin a cat? Physiologia Plantarum 142: 79-86.
Ohad I, Raanan H, Keren N, Tchernov D, Kaplan A. 2010. Light-induced changes within Photosystem II protects Microcoleus sp. in biological desert sand crusts against excess light. PLoS ONE 5: e11000.
Oren N, Raanan H, Kedem I, Turjeman A, Bronstein M, Kaplan A, Murik O. 2019. Desert cyanobacteria prepare in advance for dehydration and rewetting: the role of light and temperature sensing. Molecular Ecology 28: 2305-2320.
Peng H, Wei D, Chen G, Chen F. 2016. Transcriptome analysis reveals global regulation in response to CO2 supplementation in oleaginous microalga Coccomyxa subellipsoidea C-169. Biotechnology for Biofuels 9: 151.
Petroutsos D, Tokutsu R, Maruyama S, Flori S, Greiner A, Magneschi L, Cusant L, Kottke T, Mittag M, Hegemann P et al. 2016. A blue-light photoreceptor mediates the feedback regulation of photosynthesis. Nature 537: 563-566.
Petrushin Ivan S, Belikov Sergei I, Belykh Olga I, Tikhonova I, Chernogor Lubov I, Stajich Jason E. 2020. Draft genome sequence of the green microalga Chlorella sp. strain BAC9706, isolated from Lake Baikal, Russia. Microbiology Resource Announcements 9: e00966-20.
Pikoli MR, Sari AF, Solihat NA, Permana AH. 2019. Characteristics of tropical freshwater microalgae Micractinium conductrix, Monoraphidium sp. and Choricystis parasitica, and their potency as biodiesel feedstock. Heliyon 5: e02922.
Price MN, Dehal PS, Arkin AP. 2010. FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS ONE 5: e9490.
Raanan H, Oren N, Treves H, Keren N, Ohad I, Berkowicz SM, Hagemann M, Koch M, Shotland Y, Kaplan A. 2016. Towards clarifying what distinguishes cyanobacteria able to resurrect after desiccation from those that cannot: the photosynthetic aspect. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1857: 715-722.
Raven JA, Beardall J, Larkum AWD, Sa'Nchez-Baracaldo P. 2013. Interactions of photosynthesis with genome size and function. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 368: 20120264.
Raven JA, Knight CA, Beardall JJPIP. 2019. Genome and cell size variation across algal taxa. Perspectives in Phycology 6: 59-80.
Riaño-Pachón DM, Corrêa LG, Trejos-Espinosa R, Mueller-Roeber B. 2008. Green transcription factors: a chlamydomonas overview. Genetics 179: 31-39.
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539-542.
Roth MS, Cokus SJ, Gallaher SD, Walter A, Lopez D, Erickson E, Endelman B, Westcott D, Larabell CA, Merchant SS et al. 2017. Chromosome-level genome assembly and transcriptome of the green alga Chromochloris zofingiensis illuminates astaxanthin production. Proceedings of the National Academy of Sciences, USA 114: E4296-E4305.
Roth MS, Gallaher SD, Westcott DJ, Iwai M, Louie KB, Mueller M, Walter A, Foflonker F, Bowen BP, Ataii NN et al. 2019. Regulation of oxygenic photosynthesis during trophic transitions in the green alga Chromochloris zofingiensis. Plant Cell 31: 579-601.
Ruban AV. 2017. Quantifying the efficiency of photoprotection. Philosophical Transactions of the Royal Society B: Biological Sciences 372: 20160393.
Running JA, Huss RJ, Olson PT. 1994. Heterotrophic production of ascorbic acid by microalgae. Journal of Applied Phycology 6: 99-104.
Sambrook J, Russell DW. 2006. Purification of nucleic acids by extraction with phenol : chloroform. Cold Spring Harbor Protocols 2006: pdb.prot4455.
Seppey M, Manni M, Zdobnov EM. 2019. Busco: assessing genome assembly and annotation completeness. Methods in Molecular Biology 1962: 227-245.
Shaul O. 2017. How introns enhance gene expression. The International Journal of Biochemistry & Cell Biology 91: 145-155.
Signorile A, Sgaramella G, Bellomo F, De Rasmo D. 2019. Prohibitins: a critical role in mitochondrial functions and implication in diseases. Cell 8: 71.
Singh SP, Singh P. 2015. Effect of temperature and light on the growth of algae species: a review. Renewable and Sustainable Energy Reviews 50: 431-444.
Sperschneider J, Catanzariti A-M, Deboer K, Petre B, Gardiner DM, Singh KB, Dodds PN, Taylor JM. 2017. LOCALIZER: subcellular localization prediction of both plant and effector proteins in the plant cell. Scientific Reports 7: 44598.
Stanke M, Diekhans M, Baertsch R, Haussler D. 2008. Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24: 637-644.
Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B. 2006. Augustus: ab initio prediction of alternative transcripts. Nucleic Acids Research 34: W435-W439.
Starr RC, Zeikus JA. 1993. UTEX-the culture collection of algae at the University of Texas at Austin 1993 list of cultures. Journal of Phycology 29: 1-106.
Tatsuta T, Model K, Langer T. 2004. Formation of membrane-bound ring complexes by prohibitins in mitochondria. Molecular Biology of the Cell 16: 248-259.
Tautz D, Domazet-Lošo T. 2011. The evolutionary origin of orphan genes. Nature Reviews. Genetics 12: 692-702.
Tillich M, Lehwark P, Pellizzer T, Ulbricht-Jones ES, Fischer A, Bock R, Greiner S. 2017. GeSeq - versatile and accurate annotation of organelle genomes. Nucleic Acids Research 45: W6-W11.
Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols 7: 562-578.
Treves H, Küken A, Arrivault S, Ishihara H, Hoppe I, Erban A, Höhne M, Moraes TA, Kopka J, Szymanski J et al. 2022. Carbon flux through photosynthesis and central carbon metabolism show distinct patterns between algae, C3 and C4 plants. Nature Plants 8: 78-91.
Treves H, Murik O, Kedem I, Eisenstadt D, Meir S, Rogachev I, Szymanski J, Keren N, Orf I, Tiburcio AF et al. 2017. Metabolic flexibility underpins growth capabilities of the fastest growing alga. Current Biology 27: 2559-2567.
Treves H, Raanan H, Finkel MO, Berkowicz SM, Keren N, Kaplan A. 2013. A newly isolated Chlorella sp. from desert sand crusts exhibits a unique resistance to excess light intensity. FEMS Microbiology Ecology 86: 373-380.
Treves H, Raanan H, Kedem I, Murik O, Keren N, Zer H, Berkowicz SM, Giordano M, Norici A, Shotland Y et al. 2016. The mechanisms whereby the green alga Chlorella ohadii, isolated from desert soil crust, exhibits unparalleled photodamage resistance. New Phytologist 210: 1229-1243.
Treves H, Siemiatkowska B, Luzarowska U, Murik O, Fernandez-Pozo N, Moraes TA, Erban A, Armbruster U, Brotman Y, Kopka J et al. 2020. Multi-omics reveals mechanisms of total resistance to extreme illumination of a desert alga. Nature Plants 6: 1031-1043.
Trewick SC, Mclaughlin PJ, Allshire RC. 2005. Methylation: lost in hydroxylation? EMBO Reports 6: 315-320.
Ullrich KK, Hiss M, Rensing SA. 2015. Means to optimize protein expression in transgenic plants. Current Opinion in Biotechnology 32: 61-67.
Ungerer J, Lin P-C, Chen H-Y, Pakrasi Himadri B, Giovannoni Stephen J, Burnap R, Sherman L. 2018a. Adjustments to photosystem stoichiometry and electron transfer proteins are key to the remarkably fast growth of the cyanobacterium Synechococcus elongatus UTEX 2973. mBio 9: e02327-17.
Ungerer J, Wendt KE, Hendry JI, Maranas CD, Pakrasi HB. 2018b. Comparative genomics reveals the molecular determinants of rapid growth of the cyanobacterium Synechococcus elongatus UTEX 2973. Proceedings of the National Academy of Science USA 115: E11761-E11770.
Van Aken O, Ford E, Lister R, Huang S, Millar AH. 2016. Retrograde signalling caused by heritable mitochondrial dysfunction is partially mediated by ANAC017 and improves plant performance. The Plant Journal 88: 542-558.
Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK et al. 2014. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9: e112963.
Wang H-F, Feng L, Niu D-K. 2007. Relationship between mRNA stability and intron presence. Biochemical and Biophysical Research Communications 354: 203-208.
Weber B, Bowker M, Zhang Y, Belnap J. 2016. Natural recovery of biological soil crusts after disturbance. In: Biological soil crusts: an organizing principle in drylands. Basel, Switzerland: Springer.
Weider LJ, Elser JJ, Crease TJ, Mateos M, Cotner JB, Markow TA. 2005. The functional significance of ribosomal (r)DNA variation: impacts on the evolutionary ecology of organisms. Annual Review of Ecology, Evolution, and Systematics 36: 219-242.
Wilhelmsson PKI, Muhlich C, Ullrich KK, Rensing SA. 2017. Comprehensive genome-wide classification reveals that many plant-specific transcription factors evolved in Streptophyte algae. Genome Biology and Evolution 9: 3384-3397.
Wittkopp TM, Schmollinger S, Saroussi S, Hu W, Zhang W, Fan Q, Gallaher SD, Leonard MT, Soubeyrand E, Basset GJ et al. 2017. Bilin-dependent photoacclimation in Chlamydomonas reinhardtii. Plant Cell 29: 2711-2726.
Wood DE, Lu J, Langmead B. 2019. Improved metagenomic analysis with Kraken 2. Genome Biology 20: 257.
Wu M, Zhang H, Sun W, Li Y, Hu Q, Zhou H, Han D. 2019. Metabolic plasticity of the starchless mutant of Chlorella sorokiniana and mechanisms underlying its enhanced lipid production revealed by comparative metabolomics analysis. Algal Research 42: 101587.
Yang Z. 1997. Paml: a program package for phylogenetic analysis by maximum likelihood. Computer Applications in the Biosciences 13: 555-556.
Yu G, Wang LG, Han Y, He QY. 2012. clusterProfiler: an R package for comparing biological themes among gene clusters. Omics 16: 284-287.
Yu H, Kim J, Lee C. 2019. Nutrient removal and microalgal biomass production from different anaerobic digestion effluents with Chlorella species. Scientific Reports 9: 6123.
Zuñiga C, Li C-T, Huelsman T, Levering J, Zielinski DC, Mcconnell BO, Long CP, Knoshaug EP, Guarnieri MT, Antoniewicz MR et al. 2016. Genome-scale metabolic model for the green alga Chlorella vulgaris UTEX 395 accurately predicts phenotypes under autotrophic, heterotrophic, and mixotrophic growth conditions. Plant Physiology 172: 589-602.