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Cited by 6Marine Invertebrate Physiology and EcologyMitochondrial Function and PathologyPhysiological and biochemical adaptations

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The branched mitochondrial respiratory chain from the jellyfish Stomolophus sp2 as a probable adaptive response to environmental changes

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Nevarez-Lopez, C. A., Muhlia-Almazan, A., Gamero-Mora, E., Sanchez-Paz, A., Sastre-Velasquez, C. D., Lopez-Martinez, J.·2024·Journal of Bioenergetics and Biomembranes
DOI 10.1007/s10863-023-09999-y

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Abstract

During their long evolutionary history, jellyfish have faced changes in multiple environmental factors, to which they may selectively fix adaptations, allowing some species to survive and inhabit diverse environments. Previous findings have confirmed the jellyfish's ability to synthesize large ATP amounts, mainly produced by mitochondria, in response to environmental challenges. This study characterized the respiratory chain from the mitochondria of the jellyfish Stomolophus sp2 (previously misidentified as Stomolophus meleagris). The in-gel activity from isolated jellyfish mitochondria confirmed that the mitochondrial respiratory chain contains the four canonical complexes I to IV and F 0 F 1-ATP synthase. Specific additional activity bands, immunodetection, and mass spectrometry identification confirmed the occurrence of four alternative enzymes integrated into a branched mitochondrial respiratory chain of Stomolophus sp2: an alternative oxidase and three dehydrogenases (two NADH type II enzymes and a mitochondrial glycerol-3-phosphate dehydrogenase). The analysis of each transcript sequence, their phylogenetic relationships, and each protein's predicted models confirmed the mitochondrial alternative enzymes' identity and specific characteristics. Although no statistical differences were found among the mean values of transcript abundance of each enzyme in the transcriptomes of jellyfish exposed to three different temperatures, it was confirmed that each gene was expressed at all tested conditions. These first-time reported enzymes in cnidarians suggest the adaptative ability of jellyfish's mitochondria to display rapid metabolic responses, as previously described, to maintain energetic homeostasis and face temperature variations due to climate change.

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Research works printed but not linked: 68

  1. Aljbour SM, Zimmer M, Al-Horani FA, Kunzmann A (2019) Metabolic and oxidative stress response of the jellyfish Cassiopea sp. to changes in seawater temperature. J Sea Res 145:1–7. https://doi.org/10.1016/j.seares.2018.12.002 · DOI
  2. Aljbour SM, Zimmer M, Kunzmann A (2017) Cellular respiration, oxygen consumption, and trade-off of the jellyfish Cassiopea sp. in response to temperature change. J Sea Res 128:92–97. https://doi.org/10.1016/j.seares.2017.08.006 · DOI
  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2 · DOI · Paper page
  4. Antos-Krzeminska N, Jarmuszkiewicz W (2019) Alternative type II NAD(P)H dehydrogenases in the mitochondria of protists and fungi. Protist 170:21–37. https://doi.org/10.1016/j.protis.2018.11.001 · DOI
  5. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 71:248–254. https://doi.org/10.1016/0003-2697(76)90527-3 · DOI · Paper page
  6. Brand MD, Nicholls DG (2011) Assessing mitochondrial dysfunction in cells. Biochem J 435:297–312. https://doi.org/10.1042/BJ20110162 · DOI
  7. Brenchley PJ, Harper DAT (1999) Palaeoecology: ecosystems, environments and evolution. CRC Press, London
  8. Cabrera-Orefice A, Chiquete-Félix N, Espinasa-Jaramillo J, Rosas-Lemus M, Guerrero-Castillo S, Peña A, Uribe-Carvajal S (2014) The branched mitochondrial respiratory chain from Debaryomyces hansenii: components and supramolecular organization. Biochim Biophys Acta 1837:73–84. https://doi.org/10.1016/j.bbabio.2013.07.011 · DOI
  9. Carvalho-Saucedo L, Lopez-Martinez J, Garcia-Dominguez F, Rodriguez-Jaramillo C, Padilla-Serrato J (2011) Reproductive biology of the cannonball jellyfish Stomolophus meleagris in Las Guásimas Lagoon, Sonora, Mexico. Hidrobiologica 21:77–88
  10. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334 · DOI
  11. De Vries S, Grivell LA (1988) Purification and characterization of a rotenone-insensitive NADH: Q6 oxidoreductase from mitochondria from Saccharomyces cerevisiae. Eur J Biochem 176:377–384. https://doi.org/10.1111/j.1432-1033.1988.tb14292.x · DOI
  12. DeLano WL (2002) Pymol: an open-source molecular graphics tool. CCP4 Newsl Protein Crystallogr 40:82–92
  13. Divakaruni AS, Brand MD (2011) The regulation and physiology of mitochondrial proton leak. Physiol (Bethesda) 26:192–205. https://doi.org/10.1152/physiol.00046.2010 · DOI
  14. Drahota Z, Chowdhury SK, Floryk D, Mracek T, Wilhelm J, Rauchova H, Lenaz G, Houstek J (2002) Glycerophosphate-dependent hydrogen peroxide production by brown adipose tissue mitochondria and its activation by ferricyanide. J Bioenerg Biomembr 34:105–113. https://doi.org/10.1023/a:1015123908918 · DOI
  15. Drahota Z, Rauchova H, Jesina P, Vojtiskova A, Houstek J (2003) Glycerophosphate-dependent peroxide production by brow fat mitochondria from newborn rats. Gen Physiol Biophys 22:92–102
  16. Elthon TE, Nickels RL, McIntosh L (1989) Monoclonal antibodies to the alternative oxidase of higher plant mitochondrial. Plant Physiol 89:1311–1317. https://doi.org/10.1104/pp.89.4.1311 · DOI
  17. Felix-Torres FG, Garrido-Mora A, Sanchez-Alcudia Y, Sanchez-Martinez J, Granados-Berber AA, Ramos-Pala JL (2017) Spatial and temporal abundance and distribution of Stomolophus meleagris (Rhizostomae: Stomolophidae) in a lagoon system Southern Gulf of Mexico. Rev Biol Trop 65:1. https://doi.org/10.15517/rbt.v65i1.23727 · DOI
  18. Foster J (2014) Cambrian ocean world: ancient sea life of North America. University Press, Indiana
  19. Frolova A, Miglietta MP (2020) Insights in bloom forming jellyfish (class: Scyphozoa) in the Gulf of Mexico: environmental tolerance range and limits suggest differences in habitat preference and resistance to climate change among congeners. Front Mar Sci 7:93. https://doi.org/10.3389/fmars.2020.00093 · DOI
  20. Getino ML, Gomez DL, Garcia de Leon FJ (2019) High genetic differentiation in the edible cannonball jellyfish Cnidaria: Scyphozoa: Stomolophus spp. from the Gulf of California, Mexico. Fish Res 219:105328. https://doi.org/10.1016/j.fishres.2019.105328 · DOI
  21. Guerrero-Castillo S, Araiza-Olivera D, Cabrera-Orefice A, Espinasa-Jaramillo J, Gutierrez-Aguilar M, Luevano-Martinez LA, Zepeda-Bastida A, Uribe-Carvajal S (2011) Physiological uncoupling of mitochondrial oxidative phosphorylation. Studies in different yeast species. J Bioenerg Biomemb 43:323–331. https://doi.org/10.1007/s10863-011-9356-5 · DOI
  22. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. https://doi.org/10.1093/sysbio/syq010 · DOI · Paper page
  23. Hoang DT, Chernomor O, Von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 35:518–522. https://doi.org/10.1093/molbev/msx281 · DOI · Paper page
  24. Höhn DP, Lucas CH, Thatje S (2017) Respiratory response to temperature of three populations of Aurelia aurita polyps in northern Europe. PLoS ONE 12:e0177913. https://doi.org/10.1371/journal.pone.0177913 · DOI
  25. Holm L (2022) Dali server: structural unification of protein families. Nucleic Acids Res 50:W210–W215. https://doi.org/10.1093/nar/gkac387 · DOI
  26. Joseph-Horne T, Hollomon DW, Wood PM (2001) Fungal respiration: a fusion of standard and alternative components. Biochim Biophys Acta 1504:179–195. https://doi.org/10.1016/S0005-2728(00)00251-6 · DOI
  27. Kadenbach B, Hütteman M (2015) The subunit composition and function of mammalian cytochrome c oxidase. Mitochondrion 24:64–76. https://doi.org/10.1016/j.mito.2015.07.002 · DOI
  28. Kalyaanamoorthy S, Minh BQ, Wong TK, Von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285 · DOI · Paper page
  29. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010 · DOI · Paper page
  30. Kerscher SJ (2000) Diversity and origin of alternative NADH: ubiquinone oxidoreductases. Biochim Biophys Acta 1459:274–283. https://doi.org/10.1016/S0005-2728(00)00162-6 · DOI
  31. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. https://doi.org/10.1038/227680a0 · DOI · Paper page
  32. Lehn DA, Brown LJ, Simonson GD, Moran SM, MacDonald MJ (1994) The sequence of a human mitochondrial glycerol-3-phosphate dehydrogenase-encoding cDNA. Gene 150:417–418. https://doi.org/10.1016/0378-1119(94)90469-3 · DOI
  33. Lopez-Martinez J, Alvarez-Tello F (2013) The jellyfish fishery in Mexico. Agric Sci 4:57–61. https://doi.org/10.4236/as.2013.46A009 · DOI
  34. Maldonado-Cervantes E, Huerta-Ocampo JA, Montero-Moran GM, Barrera-Pacheco A, Espitia-Rangel E, de la Rosa APB (2014) Characterization of Amaranthus cruentus L. seed proteins by 2-DE and LC/MS–MS: identification and cloning of a novel late embryogenesis-abundant protein. J Cereal Sci 60:172–178. https://doi.org/10.1016/j.jcs.2014.02.008 · DOI
  35. Masson SWC, Hedges CP, Devaux JBL, James CS, Hickey AJR (2017) Mitochondrial glycerol 3-phosphate facilitates bumblebee pre-flight thermogenesis. Sci Rep 7:13107. https://doi.org/10.1038/s41598-017-13454-5 · DOI
  36. Matus-Ortega MG, Salmeron-Santiago KG, Flores-Herrera O, Guerra-Sanchez G, Martinez F, Rendon JL, Pardo JP (2011) The alternative NADH dehydrogenase is present in mitochondria of some animal taxa. Comp Biochem Physiol 6:256–263. https://doi.org/10.1016/j.cbd.2011.05.002 · DOI
  37. McDonald AE, Gospodaryov DV (2019) Alternative NAD(P)H dehydrogenase and alternative oxidase: proposed physiological roles in animals. Mitochondrion 45:7–17. https://doi.org/10.1016/j.mito.2018.01.009 · DOI
  38. McDonald A, Vanlerberghe GC (2004) Branched mitochondrial electron transport in the Animalia: presence of alternative oxidase in several animal phyla. IUBMB Life 56:333–341. https://doi.org/10.1080/1521-6540400000876 · DOI
  39. McDonald A, Vanlerberghe GC (2006) Origins, evolutionary history, and taxonomic distribution of alternative oxidase and plastoquino terminal oxidase. Comp Biochem Physiol 1:357–364. https://doi.org/10.1016/j.cbd.2006.08.001 · DOI
  40. McDonald A, Vanlerberghe GC, Staples JF (2009) Alternative oxidase in animals: unique characteristics and taxonomic distribution. J Exp Biol 212:2627–2634. https://doi.org/10.1242/jeb.032151 · DOI
  41. Mendez-Romero O, Rodriguez-Armenta C, Uribe-Carvajal S, Muhlia-Almazan A (2020) Functional characterization of the mitochondrial uncoupling proteins from the white shrimp Litopenaeus vannamei. Biochim Biophys Acta 1861:148209. https://doi.org/10.1016/j.bbabio.2020.148209 · DOI
  42. Mills CE (2001) Jellyfish blooms: are populations increasing globally in response to changing ocean conditions. Hydrobiologia 451:55–68. https://doi.org/10.1023/A:1011888006302 · DOI
  43. Miwa S, St-Pierre J, Partridge L, Brand MD (2003) Superoxide and hydrogen peroxide production by Drosophila mitochondria. Free Radic Biol Med 35:938–948. https://doi.org/10.1016/S0891-5849(03)00464-7 · DOI
  44. Mracek T, Drahota Z, Houstek J (2013) The function and role of the mitochondrial glycerol-3-phosphate dehydrogenase in mammalian tissues. Biochim Biophys Acta 1827:401–410. https://doi.org/10.1016/j.bbabio.2012.11.014 · DOI
  45. Mracek T, Holzerova E, Drahota Z, Kovarova N, Vrbacky M, Jesina P, Stpka P, Houstek J (2014) ROS generation and multiple forms of mammalian mitochondrial glycerol-3-phosphate dehydrogenase. Biochim Biophys Acta 1837:98–111. https://doi.org/10.1016/j.bbabio.2013.08.007 · DOI
  46. Mracek T, Pecinova A, Vrbacky M, Drahota Z, Houstek J (2009) High efficiency of ROS production by glycerophosphate dehydrogenase in mammalian mitochondria. Arch Biochem Biophys 481:30–36. https://doi.org/10.1016/j.bbamem.2008.10.011 · DOI · Paper page
  47. Nevarez-Lopez CA, Sanchez-Paz A, Lopez-Martinez J, Llera-Herrera R, Muhlia-Almazan A (2020) Metabolic response of the cannonball jellyfish Stomolophus meleagris upon short-term exposure to thermal stress. J Sea Res 166:101959. https://doi.org/10.1016/j.seares.2020.101959 · DOI
  48. Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300 · DOI · Paper page
  49. Nicholls DG, Ferguson SJ (2003) Bioenergetics 3. Academic, London
  50. Park E, Hwang D-S, Lee J-S, Song J-I, Seo T-K, Won Y-J (2012) Estimation of divergence times in cnidarian evolution based on mitochondrial protein-coding genes and the fossil record. Mol Phylogenetics Evol 62:329–345. https://doi.org/10.1016/j.ympev.2011.10.008 · DOI
  51. Rich PR, Marechal A (2010) The mitochondrial respiratory chain. Essays Biochem 47:1–23. https://doi.org/10.1042/bse0470001 · DOI
  52. Rodriguez-Armenta C, Reyes-Zamora O, De La Re-Vega E, Sanchez-Paz A, Mendez-Romero O, Gonzalez-Rios H, Muhlia-Almazan A (2021) The adaptative mitochondrial response of the whiteleg shrimp Litopenaeus vannamei to environmental challenges and pathogens. J Comp Physiol 191:629–644. https://doi.org/10.1007/s00360-021-01369-7 · DOI
  53. Rodriguez-Armenta C, Uribe-Carvajal S, Rosas-Lemus M, Chiquete-Felix N, Huerta-Ocampo JA, Muhlia-Almazan A (2018) Alternative mitochondrial respiratory chains from two crustaceans: Artemia franciscana Nauplii and the white shrimp, Litopenaeus vannamei. J Bioenerg Biomembr 50:143–152. https://doi.org/10.1007/s10863-018-9753-0 · DOI
  54. Sastre-Velasquez D (2020) Respuesta del metabolismo energético de la medusa bola de cañón Stomolophus meleagris frente a variaciones en la temperatura. MS thesis, Centro de Investigacion en Alimentacion y Desarrollo, A.C., Mexico
  55. Sokolova I (2021) Bioenergetics in environmental adaptation and stress tolerance of aquatic ectotherms: linking physiology and ecology in a multi-stressor landscape. J Exp Biol 224:jeb236802. https://doi.org/10.1242/jeb.236802 · DOI
  56. Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA (2012) Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar Environ Res 79:1–15. https://doi.org/10.1016/j.marenvres.2012.04.003 · DOI
  57. Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577. https://doi.org/10.1080/10635150701472164 · DOI
  58. Thuesen EV, Rutherford LD, Brommer PL, Garrison K, Gutowska MA, Towanda T (2005) Intra-gel oxygen promotes hypoxia tolerance of scyphomedusae. J Exp Biol 208:2475–2482. https://doi.org/10.1242/jeb.01655 · DOI
  59. Towbin H, Staehelint T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354. https://doi.org/10.1073/pnas.76.9.4350 · DOI
  60. Tward CE, Singh J, Cygelfarb W, McDonald AE (2019) Identification of the alternative oxidase gene and its expression in the copepod Tigriopus californicus. Comp Biochem Physiol 228:41–50. https://doi.org/10.1016/j.cbpb.2018.11.003 · DOI
  61. Valach M, Léveille-Kunst A, Gray MW, Burger G (2018) Respiratory chain complex I of unparalleled divergence in diplonemids. J Biol Chem 293:16043–16056. https://doi.org/10.1074/jbc.RA118.005326 · DOI
  62. Vrbacky M, Drahota Z, Mracek T, Vojtiskova A, Jesina P, Stpka P, Houstek J (2007) Respiratory chain components involved in the glycerophosphate dehydrogenase-dependent ROS production by brown adipose tissue mitochondria. Biochim Biophys Acta 1767:989–997. https://doi.org/10.1016/j.bbabio.2007.05.002 · DOI
  63. Walker JE, Dickson VK (2006) The peripheral stalk of the mitochondrial ATP synthase. Biochim Biophys Acta 1757:286–296. https://doi.org/10.1016/j.bbabio.2006.01.001 · DOI
  64. Wang W, Zhen Y, Yu Z, Shi Y, Zhao Q, Wang J, Mi T (2017) The physiological and molecular response of Aurelia sp.1 under hypoxia. Sci Rep 7:1558. https://doi.org/10.1038/s41598-017-01318-x · DOI
  65. Wittig I, Karas M, Schägger H (2007) High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Mol Cell Proteomics 6:1215–1225. https://doi.org/10.1074/mcp.M700076-MCP200 · DOI
  66. Wittig I, Schägger H (2007) Electrophoretic methods to isolated protein complexes from mitochondria. Methods Cell Biol 80:723–741. https://doi.org/10.1016/S0091-679X(06)80033-6 · DOI
  67. Zerbetto E, Vergani L, Dabbeni-Sala F (1997) Quantification of muscle mitochondrial oxidative phosphorylation enzymes via histochemical staining of blue native polyacrylamide gels. Electrophoresis 18:2059–2064. https://doi.org/10.1002/elps.1150181131 · DOI
  68. Zhao B, Gao S, Zhao M, Lv H, Song J, Wang H, Zeng Q, Liu J (2022) Mitochondrial genomic analyses provide new insights into the missing atp8 and adaptive evolution of Mytilidae. BMC Genomics 23:738. https://doi.org/10.1186/s12864-022-08940-8 · DOI

Metadata

Authors
Nevarez-Lopez, C. A., Muhlia-Almazan, A., Gamero-Mora, E., Sanchez-Paz, A., Sastre-Velasquez, C. D., & Lopez-Martinez, J.
Affiliations
Centro de Investigación en Alimentación y Desarrollo (MX)
ORCID
Venue
Journal of Bioenergetics and Biomembranes
Publisher
Springer Science and Business Media LLC
Published
2024-01-17
Volume
56
Issue
2
Pages
101-115
ISSN
  • 0145-479X (ISSN-L)
  • 1573-6881
DOI
10.1007/s10863-023-09999-y
OpenAlex
W4390953823
Cited by
6
References
4
Citations by year
2026: 3 · 2025: 1 · 2024: 2
FWCI
1.89
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Bioenergetics and Biomembranes (publishedVersion)
  • Research Square (acceptedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
Consejo Nacional de Ciencia y Tecnología (171862)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
  • Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
Keywords
jellyfish, mitochondrial respiratory chain, alternative oxidase, NADH dehydrogenase, glycerol-3-phosphate dehydrogenase, thermal adaptation, climate change, ATP synthase, mRNA levels
MeSH terms
Animals, Electron Transport Complex IV, Electron Transport, Mitochondria, Phylogeny, Scyphozoa, Mitochondrial Membranes

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Nevarez-Lopez, C. A., Muhlia-Almazan, A., Gamero-Mora, E., Sanchez-Paz, A., Sastre-Velasquez, C. D., & Lopez-Martinez, J. (2024). The branched mitochondrial respiratory chain from the jellyfish Stomolophus sp2 as a probable adaptive response to environmental changes. Journal of Bioenergetics and Biomembranes. https://doi.org/10.1007/s10863-023-09999-y