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Newly Discovered AqE Gene is Highly Conserved in Non-tetrapod Vertebrates

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Abstract

Studying the diversity of energy production pathways is important for understanding the evolutionary relationships between metabolic pathways and their biochemical precursors. The lactate/malate dehydrogenase (LDH/MDH) superfamily has been a model system for structural and functional evolution for a long time. Recently, the type-2 family of LDH/MDH (or LDH2/MDH2 oxidoreductase) has been identified. The LDH2/MDH2 oxidoreductase family is now known to have functionally more diverse enzymes than the LDH/MDH superfamily. In channel catfish, the gene encoding the LDH2/MDH2 oxidoreductase has been found (and was provisionally termed AqE). Homologs of this enzyme are predominantly present in organisms living in an aquatic environment. In this work, we studied the AqE gene distribution among non-tetrapod vertebrates. It was found that the AqE gene is present in the genomes of bony and cartilaginous fish and in the genomes of hagfishes and lampreys. In addition, it has been confirmed that in representatives of Cypriniformes, the AqE gene has been lost. AqE in representatives of Salmoniformes underwent significant deletions, which most likely led to its pseudogenization. In most orders of non-Tetrapoda vertebrates, the AqE gene remains highly conserved, suggesting that the AqE gene in aquatic vertebrates is an essential gene and undergoes rigorous selection. The AqE gene has the highest sequence similarity with the archaeal ComC gene that encodes sulfolactate dehydrogenase (SLDH). Based on the similarity of substrates, the enzyme encoded by the AqE gene is likely involved in the malate–aspartate shuttle mechanism or the biosynthesis of the energy coenzyme M equivalent.

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Data Availability

The datasets analyzed during the current study are available in the GenBank repository https://www.ncbi.nlm.nih.gov/genbank/. Some data generated or analyzed during this study are included in supplementary information files of this article.

Abbreviations

bp:

Base pair

aa:

Amino acids

ORF:

Open reading frame

WGS:

Whole-genome shotgun sequences

TSA:

Transcriptome shotgun assembly

SLDH:

Sulfolactate dehydrogenase

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  Google Scholar 

  • Bailey TL, Bodén M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208

    Article  CAS  Google Scholar 

  • Berthelot C, Brunet F, Chalopin D, Juanchich A, Bernard M, Noël B, Bento P, Da Silva C, Labadie K, Alberti A, Aury JM, Louis A, Dehais P, Bardou P, Montfort J, Klopp C, Cabau C, Gaspin C, Thorgaard GH, Boussaha M, Quillet E, Guyomard R, Galiana D, Bobe J, Volff JN, Genêt C, Wincker P, Jaillon O, Roest Crollius H, Guiguen Y (2014) The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat Commun 5:3657

    Article  Google Scholar 

  • Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA et al (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450(7167):203–218

    Article  Google Scholar 

  • Copley SD (2017) Shining a light on enzyme promiscuity. Curr Opin Struct Biol 47:167–175

    Article  CAS  Google Scholar 

  • Denger K, Cook AM (2010) Racemase activity effected by two dehydrogenases in sulfolactate degradation by Chromohalobacter salexigens: purification of (S)-sulfolactate dehydrogenase. Microbiology 156:967–974

    Article  CAS  Google Scholar 

  • Denger K, Mayer J, Buhmann M, Weinitschke S, Smits THM, Cook AM (2009) Bifurcated degradative pathway of 3-sulfolactate in Roseovarius nubinhibens ISM via sulfoacetaldehyde acetyltransferase and (S)-cysteate sulfo-lyase. J Bacteriol 191:5648–5656

    Article  CAS  Google Scholar 

  • Drouin G, Godin JR, Pagé B (2011) The genetics of vitamin C loss in vertebrates. Curr Genom 12(5):371–378

    Article  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  Google Scholar 

  • Eventoff W, Rossmann MG (1975) The evolution of dehydrogenases and kinases. CRC Crit Rev Biochem 3(2):111–140

    Article  CAS  Google Scholar 

  • Ferris SD (1984) Tetraploidy and the evolution of the catostomid Fishes. In: Turner B.J. (eds) Evolutionary Genetics of Fishes. Monographs in Evolutionary Biology. Springer:Boston, MA.

  • Goldman-Huertas B, Mitchell RF, Lapoint RT, Faucher CP, Hildebrand JG, Whiteman NK (2015) Evolution of herbivory in Drosophilidae linked to loss of behaviors, antennal responses, odorant receptors, and ancestral diet. Proc Natl Acad Sci USA 112:3026–3031

    Article  CAS  Google Scholar 

  • Graupner M, Xu H, White RH (2000) Identification of an archaeal 2-hydroxy acid dehydrogenase catalyzing reactions involved in coenzyme biosynthesis in methanoarchaea. J Bacteriol 182:3688–3692

    Article  CAS  Google Scholar 

  • Greenberg AJ, Moran JR, Coyne JA, Wu CI (2003) Ecological adaptation during incipient speciation revealed by precise gene replacement. Science 302:1754–1757

    Article  CAS  Google Scholar 

  • Hochachka PW, Somero GN. Biochemical adaptation: mechanisms and process of physiological evolution. Oxford Univesity Press;New York. 2002.

  • Holmes RS (2019) Polyploidy among salmonid aldehyde dehydrogenase genes and proteins. Chem Biol Interact 303:22–26

    Article  CAS  Google Scholar 

  • Honka E, Fabry S, Niermann T, Palm P, Hensel R (1990) Properties and primary structure of the L-malate dehydrogenase from the extremely thermophilic archaebacterium Methanothermus fervidus. Eur J Biochem 188:623–632

    Article  CAS  Google Scholar 

  • Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics. 31(8):1296–1297

    Article  Google Scholar 

  • Irimia A, Madern D, Zaccaı G, Vellieux FMD (2004) Methanoarchaeal sulfolactate dehydrogenase: prototype of a new family of NADH-dependent enzymes. The EMBO Journal 23:1234–1244

    Article  CAS  Google Scholar 

  • Jendrossek D, Kratzin HD, Steinbuchel A (1993) The Alcaligenes eutrophus ldh structural gene encodes a novel type of lactate dehydrogenase. FEMS Microbiol Lett 112:229–235

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 33:1870–1874

    Article  CAS  Google Scholar 

  • Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290(5494):1151–1155. https://doi.org/10.1126/science.290.5494.1151

    Article  CAS  Google Scholar 

  • Madern D (2002) Molecular evolution within the L-malate and L-lactate dehydrogenase super-family. J Mol Evol 54:825–840

    Article  CAS  Google Scholar 

  • McBride CS, Arguello JR, O’Meara BC (2007) Five Drosophila genomes reveal nonneutral evolution and the signature of host specialization in the chemoreceptor superfamily. Genetics 177:1395–1416

    Article  CAS  Google Scholar 

  • Moreau R, Dabrowski K (1998) Body pool and synthesis of ascorbic acid in adult sea lamprey (Petromyzon marinus): an agnathan fish with gulonolactone oxidase activity. Proc Natl Acad Sci USA 95:10279–10282

    Article  CAS  Google Scholar 

  • Muramatsu H, Mihara H, Goto M, Miyahara I, Hirotsu K, Kurihara T, Esaki N (2005) A new family of NAD(P)H-dependent oxidoreductases distinct from conventional Rossmann-fold proteins. J Biosci Bioeng 99(6):541–547

    Article  CAS  Google Scholar 

  • Nei M, Kumar S (2000) Molecular Evolution and Phylogenetics. Oxford University Press;New York.

  • Petit J, David L, Dirks R, Wiegertjes GF (2017) Genomic and transcriptomic approaches to study immunology in cyprinids: What is next? Dev Comp Immunol 75:48–62

    Article  CAS  Google Scholar 

  • Puzakova LV, Puzakov MV, Soldatov AA (2019) Gene encoding a novel enzyme of LDH2/MDH2 family is lost in plant and animal genomes during transition to land. J Mol Evol 87:52–59

    Article  CAS  Google Scholar 

  • Walsh B (2003) Population-genetic models of the fates of duplicate genes. Genetica 118(2–3):279–294

    Article  CAS  Google Scholar 

  • Zhang Y, Schofield LR, Sang C, Dey D, Ronimus RS (2017) Expression, purification, and characterization of (R)-sulfolactate dehydrogenase (ComC) from the rumen methanogen Methanobrevibacter millerae SM9. Archaea. https://doi.org/10.1155/2017/5793620

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

The reported study was funded by the Russian Foundation for Basic Research and the city of Sevastopol, Project Number 20-44-920006 (investigation of AqE gene in the genomes of cartilaginous and bony fishes) and by the Russian Academy of Sciences Research Grant No. AAAA-A18-118021490093-4 (investigation of AqE gene in the genomes of lampreys and hagfishes).

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PLV made a substantial contributions to the conception and design of the work, interpretation of data; have drafted the work. PMV made substantial contributions to the acquisition, analysis and interpretation of data. GOL made substantial contributions to the acquisition, analysis and interpretation of data. All the authors read and approved the final manuscript.

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Correspondence to Lyudmila V. Puzakova.

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The authors declare that they have no conflict of interest.

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Handling editor: Kerry Geiler-Samerotte.

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Puzakova, L.V., Puzakov, M.V. & Gostyukhina, O.L. Newly Discovered AqE Gene is Highly Conserved in Non-tetrapod Vertebrates. J Mol Evol 89, 214–224 (2021). https://doi.org/10.1007/s00239-021-09997-x

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