Phylogenetic and functional diversity of aldehyde-alcohol dehydrogenases in microalgae

Abstract

Key message

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.

Abstract

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Data availability

The ADHE1 cDNA sequence can be found in the DDBJ/EMBL/GenBank databases under the accession number ERP116271.

References

  1. 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

    CAS  Article  PubMed  Google Scholar 

  2. 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

    CAS  Article  PubMed  Google Scholar 

  3. 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

    CAS  Article  PubMed  Google Scholar 

  4. 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

    CAS  Article  PubMed  Google Scholar 

  5. 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

    CAS  Article  PubMed  Google Scholar 

  6. 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

    CAS  Article  Google Scholar 

  7. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. 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

    CAS  Article  PubMed  Google Scholar 

  9. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. Burton RM, Stadtman ER (1953) The oxidation of acetaldehyde to acetyl coenzyme A. J Biol Chem 202:873–890

    CAS  Article  Google Scholar 

  13. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. 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

    CAS  Article  PubMed  Google Scholar 

  15. 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

    CAS  Article  Google Scholar 

  16. Copley SD (2020) Evolution of new enzymes by gene duplication and divergence. FEBS J 287:1262–1283. https://doi.org/10.1111/febs.15299

    CAS  Article  PubMed  Google Scholar 

  17. 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

    CAS  Article  PubMed  Google Scholar 

  18. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. 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

    CAS  Article  PubMed  Google Scholar 

  20. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. 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

    Article  PubMed  PubMed Central  Google Scholar 

  22. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 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

    CAS  Article  Google Scholar 

  24. 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

    CAS  Article  PubMed  Google Scholar 

  25. 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

    CAS  Article  PubMed  Google Scholar 

  26. 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

    CAS  Article  Google Scholar 

  27. 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

    Article  PubMed  Google Scholar 

  28. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. 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

    CAS  Article  Google Scholar 

  32. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. 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

    CAS  Article  PubMed  Google Scholar 

  37. 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

    CAS  Article  Google Scholar 

  38. 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

    CAS  Article  PubMed  Google Scholar 

  39. 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

    CAS  Article  PubMed  Google Scholar 

  40. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Pringsheim EG (1955) The Genus Polytomella*. J Protozool 2:137–145. https://doi.org/10.1111/j.1550-7408.1955.tb02413.x

    Article  Google Scholar 

  42. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. 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

    CAS  Article  PubMed  Google Scholar 

  46. 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

    Article  PubMed  Google Scholar 

  47. 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

    Article  PubMed  Google Scholar 

  48. 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

    Article  PubMed  Google Scholar 

  49. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. 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

    CAS  Article  PubMed  Google Scholar 

  52. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. 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

    CAS  Article  PubMed  Google Scholar 

  55. 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

    CAS  Article  PubMed  Google Scholar 

  56. 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

    CAS  Article  Google Scholar 

  57. 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

    CAS  Article  PubMed  Google Scholar 

  58. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  59. 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

    CAS  Article  PubMed  Google Scholar 

  60. 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

    CAS  Article  PubMed  Google Scholar 

  61. 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

    CAS  Article  PubMed  Google Scholar 

  62. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  63. 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

    CAS  Article  PubMed  Google Scholar 

  64. Wise DL (1955) Carbon sources for Polytomella caeca. J Protozool 2:156–158. https://doi.org/10.1111/j.1550-7408.1955.tb02416.x

    CAS  Article  Google Scholar 

  65. 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

    CAS  Article  Google Scholar 

  66. 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

    CAS  Article  PubMed  Google Scholar 

  67. Wise DL (1970) Effect of acetaldehyde on growth in succinate media and labeling RNA with 14C succinate in Polytomella caeca. J Protozool 17:1970

    Article  Google Scholar 

  68. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  69. 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

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Dr. David R. Smith (Dalhousie University, Canada) for sharing genome assemblies of P. magna, P. capuana, P. piriformis and P. parva.

Funding

This work was supported by the Centre National de la Recherche Scientifique (CNRS), Aix-Marseille Université (AMU) and the LABEX Dynamo (ANR-11-LABX-0011-01). Proteomic experiments were partly supported by the Agence Nationale de la Recherche (ANR-10-INBS-08-01 ProFI Grant).

Author information

Affiliations

Authors

Contributions

AA and RvL conceived the study, designed and conducted the experiments. OV, NJT, BL and AA assembled and annotated genomes. YC and SB performed the proteomic studies. AA, RvL, WN and OV performed the bioinformatics analyses. AA, RvL and OV wrote the manuscript and generated the figures. All authors participated and approved the final version of the manuscript.

Corresponding author

Correspondence to Ariane Atteia.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

van Lis, R., Couté, Y., Brugière, S. et al. Phylogenetic and functional diversity of aldehyde-alcohol dehydrogenases in microalgae. Plant Mol Biol 105, 497–511 (2021). https://doi.org/10.1007/s11103-020-01105-9

Download citation

Keywords

  • Alcohol dehydrogenase (ADH)
  • Bifunctional enzyme
  • Gene duplication
  • Polytomella
  • Spirosome