Phylogenetic and functional diversity of aldehyde-alcohol dehydrogenases in microalgae.
Alcohol Dehydrogenase
/ classification
Aldehyde Dehydrogenase
/ classification
Algal Proteins
/ genetics
Amino Acid Sequence
Chlorophyta
/ enzymology
Genetic Variation
Mass Spectrometry
/ methods
Microalgae
/ enzymology
Phylogeny
Proteomics
/ methods
Sequence Analysis, DNA
/ methods
Sequence Homology, Amino Acid
Alcohol dehydrogenase (ADH)
Bifunctional enzyme
Gene duplication
Polytomella
Spirosome
Journal
Plant molecular biology
ISSN: 1573-5028
Titre abrégé: Plant Mol Biol
Pays: Netherlands
ID NLM: 9106343
Informations de publication
Date de publication:
Mar 2021
Mar 2021
Historique:
received:
12
08
2020
accepted:
10
12
2020
pubmed:
9
1
2021
medline:
2
3
2021
entrez:
8
1
2021
Statut:
ppublish
Résumé
The study shows the biochemical and enzymatic divergence between the two aldehyde-alcohol dehydrogenases of the alga Polytomella sp., shedding light on novel aspects of the enzyme evolution amid unicellular eukaryotes. Aldehyde-alcohol dehydrogenases (ADHEs) are large metalloenzymes that typically perform the two-step reduction of acetyl-CoA into ethanol. These enzymes consist of an N-terminal acetylating aldehyde dehydrogenase domain (ALDH) and a C-terminal alcohol dehydrogenase (ADH) domain. ADHEs are present in various bacterial phyla as well as in some unicellular eukaryotes. Here we focus on ADHEs in microalgae, a diverse and polyphyletic group of plastid-bearing unicellular eukaryotes. Genome survey shows the uneven distribution of the ADHE gene among free-living algae, and the presence of two distinct genes in various species. We show that the non-photosynthetic Chlorophyte alga Polytomella sp. SAG 198.80 harbors two genes for ADHE-like enzymes with divergent C-terminal ADH domains. Immunoblots indicate that both ADHEs accumulate in Polytomella cells growing aerobically on acetate or ethanol. ADHE1 of ~ 105-kDa is found in particulate fractions, whereas ADHE2 of ~ 95-kDa is mostly soluble. The study of the recombinant enzymes revealed that ADHE1 has both the ALDH and ADH activities, while ADHE2 has only the ALDH activity. Phylogeny shows that the divergence occurred close to the root of the Polytomella genus within a clade formed by the majority of the Chlorophyte ADHE sequences, next to the cyanobacterial clade. The potential diversification of function in Polytomella spp. unveiled here likely took place after the loss of photosynthesis. Overall, our study provides a glimpse at the complex evolutionary history of the ADHE in microalgae which includes (i) acquisition via different gene donors, (ii) gene duplication and (iii) independent evolution of one of the two enzymatic domains.
Identifiants
pubmed: 33415608
doi: 10.1007/s11103-020-01105-9
pii: 10.1007/s11103-020-01105-9
doi:
Substances chimiques
Algal Proteins
0
Alcohol Dehydrogenase
EC 1.1.1.1
Aldehyde Dehydrogenase
EC 1.2.1.3
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
497-511Subventions
Organisme : Agence Nationale de la Recherche
ID : ANR-11-LABX-0011-01
Organisme : Agence Nationale de la Recherche
ID : ANR-10-INBS-08-01 ProFI grant
Références
Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kröger N, Lau WWY, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86. https://doi.org/10.1126/science.1101156
doi: 10.1126/science.1101156
pubmed: 15459382
Atteia A, Dreyfus G, González-Halphen D (1997) Characterization of the alpha and beta-subunits of the F0F1-ATPase from the alga Polytomella spp., a colorless relative of Chlamydomonas reinhardtii. Biochim Biophys Acta 1320:275–284. https://doi.org/10.1016/s0005-2728(97)00031-5
doi: 10.1016/s0005-2728(97)00031-5
pubmed: 9230922
Atteia A, van Lis R, Ramírez J, González-Halphen D (2000) Polytomella spp. growth on ethanol. Extracellular pH affects the accumulation of mitochondrial cytochrome c550. Eur J Biochem 267:2850–2858. https://doi.org/10.1046/j.1432-1327.2000.01288.x
doi: 10.1046/j.1432-1327.2000.01288.x
pubmed: 10806382
Atteia A, van Lis R, Mendoza-Hernández G, Henze K, Martin W, Riveros-Rosas H, González-Halphen D (2003) Bifunctional aldehyde/alcohol dehydrogenase (ADHE) in chlorophyte algal mitochondria. Plant Mol Biol 53:175–188. https://doi.org/10.1023/B:PLAN.0000009274.19340.36
doi: 10.1023/B:PLAN.0000009274.19340.36
pubmed: 14756315
Atteia A, van Lis R, Gelius-Dietrich G, Adrait A, Garin J, Joyard J, Rolland N, Martin W (2006) Pyruvate formate-lyase and a novel route of eukaryotic ATP synthesis in Chlamydomonas mitochondria. J Biol Chem 281:9909–9918. https://doi.org/10.1074/jbc.M507862200
doi: 10.1074/jbc.M507862200
pubmed: 16452484
Atteia A, van Lis R, Tielens AGM, Martin WF (2013) Anaerobic energy metabolism in unicellular photosynthetic eukaryotes. Biochim Biophys Acta Bioenerg 1827:210–223. https://doi.org/10.1016/j.bbabio.2012.08.002
doi: 10.1016/j.bbabio.2012.08.002
Bairoch A (1992) Prosite: a dictionary of sites and patterns in proteins. Nucleic Acids Res 20:2013–2018. https://doi.org/10.1093/nar/20.suppl.2013
doi: 10.1093/nar/20.suppl.2013
pubmed: 1598232
pmcid: 333978
Blaby-Haas CE, Merchant SS (2019) Comparative and functional algal genomics. Annu Rev Plant Biol 70:605–638. https://doi.org/10.1146/annurev-arplant-050718-095841
doi: 10.1146/annurev-arplant-050718-095841
pubmed: 30822111
Bouyssié D, Hesse A-M, Mouton-Barbosa E, Rompais M, Macron C, Carapito C, Gonzalez de Peredo A, Couté Y, Dupierris V, Burel A, Menetrey J-P, Kalaitzakis A, Poisat J, Romdhani A, Burlet-Schiltz O, Cianférani S, Garin J, Bruley C (2020) Proline: an efficient and user-friendly software suite for large-scale proteomics. Bioinformatics 36(10):3148–3155. https://doi.org/10.1093/bioinformatics/btaa118
doi: 10.1093/bioinformatics/btaa118
pubmed: 32096818
pmcid: 7214047
Boxma B, Voncken F, Jannink S, van Alen T, Akhmanova A, van Weelden SWH, van Hellemond JJ, Ricard G, Huynen M, Tielens AGM, Hackstein JHP (2004) The anaerobic chytridiomycete fungus Piromyces sp. E2 produces ethanol via pyruvate:formate lyase and an alcohol dehydrogenase E. Mol Microbiol 51:1389–1399. https://doi.org/10.1046/j.1365-2958.2003.03912.x
doi: 10.1046/j.1365-2958.2003.03912.x
pubmed: 14982632
pmcid: 14982632
Bruchhaus I, Tannich E (1994) Purification and molecular characterization of the NAD(+)-dependent acetaldehyde/alcohol dehydrogenase from Entamoeba histolytica. Biochem J 303(Pt 3):743–748. https://doi.org/10.1042/bj3030743
doi: 10.1042/bj3030743
pubmed: 7980441
pmcid: 1137609
Burton RM, Stadtman ER (1953) The oxidation of acetaldehyde to acetyl coenzyme A. J Biol Chem 202:873–890
doi: 10.1016/S0021-9258(18)66200-3
Catalanotti C, Dubini A, Subramanian V, Yang W, Magneschi L, Mus F, Seibert M, Posewitz MC, Grossman AR (2012) Altered fermentative metabolism in Chlamydomonas reinhardtii mutants lacking pyruvate formate lyase and both pyruvate formate lyase and alcohol dehydrogenase. Plant Cell 24:692–707. https://doi.org/10.1105/tpc.111.093146
doi: 10.1105/tpc.111.093146
pubmed: 22353371
pmcid: 3315241
Cederbaum AI, Lieber CS, Rubin E (1973) Effect of acetaldehyde on activity of shuttles for the transport of reducing equivalents into the mitochondria. FEBS Lett 37:89–92. https://doi.org/10.1016/0014-5793(73)80432-6
doi: 10.1016/0014-5793(73)80432-6
pubmed: 4356722
Cederbaum AI, Lieber CS, Rubin E (1974) The effect of acetaldehyde on mitochondrial function. Arch Biochem Biophys 161:26–39. https://doi.org/10.1016/0003-9861(74)90231-8
doi: 10.1016/0003-9861(74)90231-8
Copley SD (2020) Evolution of new enzymes by gene duplication and divergence. FEBS J 287:1262–1283. https://doi.org/10.1111/febs.15299
doi: 10.1111/febs.15299
pubmed: 32250558
Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016. https://doi.org/10.1006/jmbi.2000.3903
doi: 10.1006/jmbi.2000.3903
pubmed: 10891285
Fukasawa Y, Tsuji J, Fu S-C, Tomii K, Horton P, Imai K (2015) MitoFates: improved prediction of mitochondrial targeting sequences and their cleavage sites. Mol Cell Proteomics 14:1113–1126. https://doi.org/10.1074/mcp.M114.043083
doi: 10.1074/mcp.M114.043083
pubmed: 25670805
pmcid: 4390256
Funes S, Davidson E, Gonzalo Claros M, van Lis R, Pérez-Martínez X, Vázquez-Acevedo M, King MP, González-Halphen D (2002) The typically mitochondrial DNA-encoded ATP6 subunit of the F 1 F 0 -ATPase is encoded by a nuclear gene in Chlamydomonas reinhardtii. J Biol Chem 277:6051–6058. https://doi.org/10.1074/jbc.M109993200
doi: 10.1074/jbc.M109993200
pubmed: 11744727
Gould SB, Garg SG, Handrich M, Nelson-Sathi S, Gruenheit N, Tielens AGM, Martin WF (2019) Adaptation to life on land at high O(2) via transition from ferredoxin-to NADH-dependent redox balance. Proc Biol Sci 286:20191491. https://doi.org/10.1098/rspb.2019.1491
doi: 10.1098/rspb.2019.1491
pubmed: 31431166
pmcid: 6732389
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. Front Bioeng Biotechnol 6:37. https://doi.org/10.3389/fbioe.2018.00037
doi: 10.3389/fbioe.2018.00037
pubmed: 29675409
pmcid: 5895722
Hemschemeier A, Jacobs J, Happe T (2008) Biochemical and physiological characterization of the pyruvate formate-lyase Pfl1 of Chlamydomonas reinhardtii a typically bacterial enzyme in a eukaryotic alga. Eukaryot Cell 7:518–526. https://doi.org/10.1128/EC.00368-07
doi: 10.1128/EC.00368-07
pubmed: 18245276
pmcid: 2268514
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8:275–282. https://doi.org/10.1093/bioinformatics/8.3.275
doi: 10.1093/bioinformatics/8.3.275
Kawata T, Masuda K, Yoshino K (1975) Presence of fine spirals (spirosomes) in Lactobacillus fermenti and Lactobacillus casei. Jpn J Microbiol 19:225–227. https://doi.org/10.1111/j.1348-0421.1975.tb00872.x
doi: 10.1111/j.1348-0421.1975.tb00872.x
pubmed: 809611
Kessler D, Leibrecht I, Knappe J (1991) Pyruvate-formate-lyase-deactivase and acetyl-CoA reductase activities of Escherichia coli reside on a polymeric protein particle encoded by adhE. FEBS Lett 281:59–63. https://doi.org/10.1016/0014-5793(91)80358-a
doi: 10.1016/0014-5793(91)80358-a
pubmed: 2015910
Kessler D, Herth W, Knappe J (1992) Ultrastructure and pyruvate formate-lyase radical quenching property of the multienzymic AdhE protein of Escherichia coli. J Biol Chem 267:18073–18079
doi: 10.1016/S0021-9258(19)37154-6
Kim KM, Park J-H, Bhattacharya D, Yoon HS (2014) Applications of next-generation sequencing to unravelling the evolutionary history of algae. Int J Syst Evol Microbiol 64:333–345. https://doi.org/10.1099/ijs.0.054221-0
doi: 10.1099/ijs.0.054221-0
pubmed: 24505071
Kim G, Azmi L, Jang S, Jung T, Hebert H, Roe AJ, Byron O, Song J-J (2019) Aldehyde-alcohol dehydrogenase forms a high-order spirosome architecture critical for its activity. Nat Commun 10:4527. https://doi.org/10.1038/s41467-019-12427-8
doi: 10.1038/s41467-019-12427-8
pubmed: 31586059
pmcid: 6778083
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
doi: 10.1093/molbev/msw054
pubmed: 27004904
pmcid: 27004904
Kurylo CM, Parks MM, Juette MF, Zinshteyn B, Altman RB, Thibado JK, Vincent CT, Blanchard SC (2018) Endogenous rRNA sequence variation can regulate stress response gene expression and phenotype. Cell Rep 25:236-248.e6. https://doi.org/10.1016/j.celrep.2018.08.093
doi: 10.1016/j.celrep.2018.08.093
pubmed: 30282032
pmcid: 6312700
Lees GJ, Jago GR (1978) Role of acetaldehyde in metabolism: a review 1. Enzymes catalyzing reactions involving acetaldehyde. J Dairy Sci 61:1205–1215. https://doi.org/10.3168/jds.S0022-0302(78)83708-4
doi: 10.3168/jds.S0022-0302(78)83708-4
Magneschi L, Catalanotti C, Subramanian V, Dubini A, Yang W, Mus F, Posewitz MC, Seibert M, Perata P, Grossman AR (2012) A mutant in the ADH1 gene of Chlamydomonas reinhardtii elicits metabolic restructuring during anaerobiosis. Plant Physiol 158:1293–1305. https://doi.org/10.1104/pp.111.191569
doi: 10.1104/pp.111.191569
pubmed: 22271746
pmcid: 3291268
Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Grigoriev IV, Rokhsar DS, Grossman AR, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernández E, Fukuzawa H, González-Ballester D, González-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riaño-Pachón DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martínez D, Ngau WCA, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–251. https://doi.org/10.1126/science.1143609
doi: 10.1126/science.1143609
pubmed: 17932292
pmcid: 2875087
Montella C, Bellsolell L, Pérez-Luque R, Badía J, Baldoma L, Coll M, Aguilar J (2005) Crystal structure of an iron-dependent group III dehydrogenase that interconverts L-lactaldehyde and L-1,2-propanediol in Escherichia coli. J Bacteriol 187:4957–4966. https://doi.org/10.1128/JB.187.14.4957-4966.2005
doi: 10.1128/JB.187.14.4957-4966.2005
pubmed: 15995211
pmcid: 1169507
Müller M, Mentel M, van Hellemond JJ, Henze K, Woehle C, Gould SB, Yu R-Y, van der Giezen M, Tielens AGM, Martin WF (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76:444–495. https://doi.org/10.1128/MMBR.05024-11
doi: 10.1128/MMBR.05024-11
pubmed: 22688819
pmcid: 22688819
Mus F, Dubini A, Seibert M, Posewitz MC, Grossman AR (2007) Anaerobic acclimation in Chlamydomonas reinhardtii: anoxic gene expression, hydrogenase induction, and metabolic pathways. J Biol Chem 282:25475–25486. https://doi.org/10.1074/jbc.M701415200
doi: 10.1074/jbc.M701415200
pubmed: 17565990
Nelson DR, Chaiboonchoe A, Fu W, Hazzouri KM, Huang Z, Jaiswal A, Daakour S, Mystikou A, Arnoux M, Sultana M, Salehi-Ashtiani K (2019) Potential for heightened sulfur-metabolic capacity in coastal subtropical microalgae. Science 11:450–465. https://doi.org/10.1016/j.isci.2018.12.035
doi: 10.1016/j.isci.2018.12.035
Pietrocola F, Galluzzi L, Bravo-San Pedro JM, Madeo F, Kroemer G (2015) Acetyl coenzyme A: a central metabolite and second messenger. Cell Metab 21:805–821. https://doi.org/10.1016/j.cmet.2015.05.014
doi: 10.1016/j.cmet.2015.05.014
pubmed: 26039447
Piganeau G, Grimsley N, Moreau H (2011) Genome diversity in the smallest marine photosynthetic eukaryotes. Res Microbiol 162:570–577. https://doi.org/10.1016/j.resmic.2011.04.005
doi: 10.1016/j.resmic.2011.04.005
pubmed: 21540104
Pony P, Rapisarda C, Terradot L, Marza E, Fronzes R (2020) Filamentation of the bacterial bi-functional alcohol/aldehyde dehydrogenase AdhE is essential for substrate channeling and enzymatic regulation. Nat Commun 11:1426. https://doi.org/10.1038/s41467-020-15214-y
doi: 10.1038/s41467-020-15214-y
pubmed: 32188856
pmcid: 7080775
Pringsheim EG (1955) The Genus Polytomella*. J Protozool 2:137–145. https://doi.org/10.1111/j.1550-7408.1955.tb02413.x
doi: 10.1111/j.1550-7408.1955.tb02413.x
Radakovits R, Jinkerson RE, Fuerstenberg SI, Tae H, Settlage RE, Boore JL, Posewitz MC (2012) Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nat Commun 3:686. https://doi.org/10.1038/ncomms1688
doi: 10.1038/ncomms1688
pubmed: 22353717
pmcid: 3293424
Roof DM, Roth JR (1992) Autogenous regulation of ethanolamine utilization by a transcriptional activator of the eut operon in Salmonella typhimurium. J Bacteriol 174:6634–6643. https://doi.org/10.1128/jb.174.20.6634-6643.1992
doi: 10.1128/jb.174.20.6634-6643.1992
pubmed: 1328159
pmcid: 207641
Rosenthal B, Mai Z, Caplivski D, Ghosh S, de la Vega H, Graf T, Samuelson J (1997) Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoan parasite Entamoeba histolytica. J Bacteriol 179:3736–3745. https://doi.org/10.1128/jb.179.11.3736-3745.1997
doi: 10.1128/jb.179.11.3736-3745.1997
pubmed: 9171424
pmcid: 179172
Salvetti A, Couté Y, Epstein A, Arata L, Kraut A, Navratil V, Bouvet P, Greco A (2016) Nuclear functions of nucleolin through global proteomics and interactomic approaches. J Proteome Res 15:1659–1669. https://doi.org/10.1021/acs.jproteome.6b00126
doi: 10.1021/acs.jproteome.6b00126
pubmed: 27049334
Sánchez LB (1998) Aldehyde dehydrogenase (CoA-acetylating) and the mechanism of ethanol formation in the amitochondriate protist, Giardia lamblia. Arch Biochem Biophys 354:57–64. https://doi.org/10.1006/abbi.1998.0664
doi: 10.1006/abbi.1998.0664
pubmed: 9633598
Schägger H, von Jagow G (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199:223–231. https://doi.org/10.1016/0003-2697(91)90094-a
doi: 10.1016/0003-2697(91)90094-a
pubmed: 1812789
Schägger H, Cramer WA, von Jagow G (1994) Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal Biochem 217:220–230. https://doi.org/10.1006/abio.1994.1112
doi: 10.1006/abio.1994.1112
pubmed: 8203750
Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M (2011) Global quantification of mammalian gene expression control. Nature 473:337–342. https://doi.org/10.1038/nature10098
doi: 10.1038/nature10098
pubmed: 21593866
pmcid: 21593866
Shasmal M, Dey S, Shaikh TR, Bhakta S, Sengupta J (2016) E. coli metabolic protein aldehyde-alcohol dehydrogenase-E binds to the ribosome: a unique moonlighting action revealed. Sci Rep 6:19936. https://doi.org/10.1038/srep19936
doi: 10.1038/srep19936
pubmed: 26822933
pmcid: 4731797
Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: A tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4:1581–1590. https://doi.org/10.1002/pmic.200300776
doi: 10.1002/pmic.200300776
pubmed: 15174128
Smith DR, Lee RW (2014) A plastid without a genome: evidence from the nonphotosynthetic green algal genus Polytomella. Plant Physiol 164:1812–1819. https://doi.org/10.1104/pp.113.233718
doi: 10.1104/pp.113.233718
pubmed: 24563281
pmcid: 3982744
Smith DR, Hua J, Archibald JM, Lee RW (2013) Palindromic genes in the linear mitochondrial genome of the nonphotosynthetic green alga Polytomella magna. Genome Biol Evol 5:1661–1667. https://doi.org/10.1093/gbe/evt122
doi: 10.1093/gbe/evt122
pubmed: 23940100
pmcid: 3787674
Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41:207–234. https://doi.org/10.1016/j.pep.2005.01.016
doi: 10.1016/j.pep.2005.01.016
pubmed: 15915565
Tardif M, Atteia A, Specht M, Cogne G, Rolland N, Brugière S, Hippler M, Ferro M, Bruley C, Peltier G, Vallon O, Cournac L (2012) PredAlgo: a new subcellular localization prediction tool dedicated to green algae. Mol Biol Evol 29:3625–3639. https://doi.org/10.1093/molbev/mss178
doi: 10.1093/molbev/mss178
pubmed: 22826458
Toth J, Ismaiel AA, Chen JS (1999) The ald gene, encoding a coenzyme A-acylating aldehyde dehydrogenase, distinguishes Clostridium beijerinckii and two other solvent-producing clostridia from Clostridium acetobutylicum. Appl Environ Microbiol 65:4973–4980
doi: 10.1128/AEM.65.11.4973-4980.1999
van Lis R, González-Halphen D, Atteia A (2005) Divergence of the mitochondrial electron transport chains from the green alga Chlamydomonas reinhardtii and its colorless close relative Polytomella sp. Biochim Biophys Acta 1708:23–34. https://doi.org/10.1016/j.bbabio.2004.12.010
doi: 10.1016/j.bbabio.2004.12.010
pubmed: 15949981
van Lis R, Mendoza-Hernández G, Groth G, Atteia A (2007) New insights into the unique structure of the F0F 1-ATP synthase from the chlamydomonad algae Polytomella sp. and Chlamydomonas reinhardtii. Plant Physiol 144:1190–1199. https://doi.org/10.1104/pp.106.094060
doi: 10.1104/pp.106.094060
pubmed: 17468226
pmcid: 1914207
van Lis R, Baffert C, Couté Y, Nitschke W, Atteia A (2013) Chlamydomonas reinhardtii chloroplasts contain a homodimeric pyruvate: ferredoxin oxidoreductase that functions with FDX1. Plant Physiol 161:57–71. https://doi.org/10.1104/pp.112.208181
doi: 10.1104/pp.112.208181
pubmed: 23154536
van Lis R, Popek M, Couté Y, Kosta A, Drapier D, Nitschke W, Atteia A (2017) Concerted up-regulation of aldehyde/alcohol dehydrogenase (ADHE) and starch in Chlamydomonas reinhardtii increases survival under dark anoxia. J Biol Chem 292:2395–2410. https://doi.org/10.1074/jbc.M116.766048
doi: 10.1074/jbc.M116.766048
pubmed: 28007962
van Lis R, Brugière S, Baffert C, Couté Y, Nitschke W, Atteia A (2020) Hybrid cluster proteins in a photosynthetic microalga. FEBS J 287:721–735. https://doi.org/10.1111/febs.15025
doi: 10.1111/febs.15025
pubmed: 31361397
Wang D, Ning K, Li J, Hu J, Han D, Wang H, Zeng X, Jing X, Zhou Q, Su X, Chang X, Wang A, Wang W, Jia J, Wei L, Xin Y, Qiao Y, Huang R, Chen J, Han B, Yoon K, Hill RT, Zohar Y, Chen F, Hu Q, Xu J (2014) Nannochloropsis genomes reveal evolution of microalgal oleaginous traits. PLoS Genet 10:e1004094. https://doi.org/10.1371/journal.pgen.1004094
doi: 10.1371/journal.pgen.1004094
pubmed: 24415958
pmcid: 3886936
Wessel D, Flügge UI (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138:141–143. https://doi.org/10.1016/0003-2697(84)90782-6
doi: 10.1016/0003-2697(84)90782-6
pubmed: 6731838
Wise DL (1955) Carbon sources for Polytomella caeca. J Protozool 2:156–158. https://doi.org/10.1111/j.1550-7408.1955.tb02416.x
doi: 10.1111/j.1550-7408.1955.tb02416.x
Wise DL (1959) Carbon nutrition and metabolism of Polytomella caeca. J Protozool 6:19–23. https://doi.org/10.1111/j.1550-7408.1959.tb03921.x
doi: 10.1111/j.1550-7408.1959.tb03921.x
Wise DL (1968) Effects of acetaldehyde on growth and biosynthesis in an algal flagellate Polytomella caeca. J Protozool 15:528–531. https://doi.org/10.1111/j.1550-7408.1968.tb02169.x
doi: 10.1111/j.1550-7408.1968.tb02169.x
pubmed: 5703081
Wise DL (1970) Effect of acetaldehyde on growth in succinate media and labeling RNA with 14C succinate in Polytomella caeca. J Protozool 17:1970
doi: 10.1111/j.1550-7408.1970.tb02353.x
Wu T, Li L, Jiang X, Yang Y, Song Y, Chen L, Xu X, Shen Y, Gu Y (2019) Sequencing and comparative analysis of three Chlorella genomes provide insights into strain-specific adaptation to wastewater. Sci Rep 9:9514. https://doi.org/10.1038/s41598-019-45511-6
doi: 10.1038/s41598-019-45511-6
pubmed: 31267025
pmcid: 6606587
Zimorski V, Martin WF (2014) Subcellular targeting of proteins and pathways during evolution. New Phytol 201:1–2. https://doi.org/10.1111/nph.12566
doi: 10.1111/nph.12566
pubmed: 24274788