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Hypoxia tolerance in two amazon cichlids: mitochondrial respiration and cellular metabolism adjustments are result of species environmental preferences and distribution

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Abstract

The amazon fishes’ responses to hypoxia seem to be related to the Amazon basin diversity of aquatic environments, which present drastic daily and seasonal variations in the dissolved oxygen concentration. Among these fishes’ adaptation to hypoxia, behavioral, metabolic, physiological, and biochemical responses are well known for some species. In this work, we aimed to identify how two different aquatic environments, normoxic forest streams and hypoxic lakes, dictate the responses to hypoxia for two cichlid species, Mesonauta festivus and Aequidens pallidus. In our results, we found that A. pallidus is less tolerant to hypoxia, which seems to be related to this animal’s natural normoxic environment. Even though this species modulated the mitochondrial respiration in order to improve the oxygen use, it also showed a lower decrease in metabolic rate when exposed to hypoxia and no activation of the anaerobic metabolism. Instead, M. festivus showed a higher decrease in metabolic rate and an activation of the anaerobic metabolism. Our data reveal that the natural dissolved oxygen influences the hypoxia tolerance and the species’ tolerance is related to its ability to perform metabolic depression. The interest results are the absence of mitochondrial respiration influences in these processes. The results observed with A. pallidus bring to light also the importance of preserving the forests, in which streams hold very specialized species acclimated to normoxia and lower temperature. The importance of hypoxia tolerance is, thus, important to keep fish assemblage and is thought to be a strong driver of fish biodiversity.

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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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References

  • Almeida-Val VMF, Val AL, Hochachka PW (1993) Hypoxia tolerance in Amazon fishes: status of an under-explored biological “goldmine.” Surviving Hypoxia: Mechanisms of Control and Adaptation. CRC Press, Boca Raton, pp 435–445

  • Almeida-Val VM, Farias IP, Silva MN, Duncan WP, Val AL (1995) Biochemical adjustments to hypoxia by Amazon cichlids. Braz J Med Biol Res 28(11–12):1257–63

  • Almeida-Val VMF, Val AL, Duncan WP, Souza FC, Paula-Silva MN, Land S (2000) Scaling effects on hypoxia tolerance in the Amazon fish Astronotus ocellatus (Perciformes: Cichlidae): contribution of tissue enzyme levels. Comp Biochem Physiol B Biochem Mol Biol 125(2):219–226

    Article  CAS  Google Scholar 

  • Almeida-Val VMF, Hochachka PW (1995) Air-breathing fishes: metabolic biochemistry of the first diving vertebrates. Bioche and mol bio of fish. Vol. 5, pp. 45–55. Elsevier. https://doi.org/10.1016/S1873-0140(06)80029-9

  • Anjos Mb, De Oliveira Rr, Zuanon J (2008) Hypoxic environments as refuge against predatory fish in the Amazonian floodplains. Braz J Biol 68:45–50. https://doi.org/10.1590/S1519-69842008000100007

  • Araújo JDA, Ghelfi A, Val AL (2017) Triportheus albus Cope, 1872 in the Blackwater, Clearwater, and Whitewater of the Amazon: a case of phenotypic plasticity? Front Genet 8:114. https://doi.org/10.3389/fgene.2017.00114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Araújo-Lima CARM, Agostinho AA, Fabré NN (1995) Trophic aspects of fish communities in Brazilian rivers and reservoirs. In: Tundisi JB, Bicudo CEM, Matsumara-Tundisi T (eds) Limnology in Brazil. ABC/SBL, São Paulo, pp 105–136

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the protein-dye binding. Anal Biochem 72:248–254

  • Cadenas S (2018) ROS and redox signaling in myocardial ischemia-reperfusion injury and cardioprotection. Free Radic Biol Med 117:76–89. https://doi.org/10.1016/j.freeradbiomed.2018.01.024

    Article  CAS  Google Scholar 

  • Campos DF, Braz-Mota S, Heinrichs-Caldas W, Val AL, Almeida-Val VMF (2020). Control of heart mitochondrial respiration in Amazon fish with different respiratory strategies In: ADAPTA: Adaptations of aquatic biota. Short note vol. 2, 11–15.

  • Castro JS, Braz-Mota S, Campos DF, Souza SS, Val AL (2020) High temperature, pH, and hypoxia cause oxidative stress and impair the spermatic performance of the Amazon fish Colossoma macropomum. Front Physiol 11:772. https://doi.org/10.3389/fphys.2020.00772

    Article  PubMed  PubMed Central  Google Scholar 

  • Chowdhury S, Saikia SK (2020) Oxidative stress in fish: a review. J. Sci. Res. 12:145–160. https://doi.org/10.3329/jsr.v12i1.41716

    Article  Google Scholar 

  • Chippari-Gomes AR, Gomes LC, Lopes NP, Val AL, Almeida-Val VMF (2005) Metabolic adjustments in two Amazonian cichlids exposed to hypoxia and anoxia. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 141(3):347–355

  • Costa FRC, Zuanon JAS, Baccaro FB, de Almeida JS, da S Menger J, Souza JLP, Borba GC, Esteban EJL, Bertin VM, Gerolamo CS, Nogueira A, de Castilho CV (2020) Effects of climate change on Central Amazonian forests: a two decades synthesis of monitoring tropical biodiversity. Oecologia Aust 24:317–335. https://doi.org/10.4257/oeco.2020.2402.07

    Article  Google Scholar 

  • De Boeck G, Wood CM, Iftikar FI, Matey V, Scott G, Paula-Silva MN, Almeida-Val VMF, Val AL (2013) Interactions between hypoxia tolerance and food deprivation in Amazonian oscars, Astronotus ocellatus J Exp Biol 216:4590–4600. https://doi.org/10.1242/jeb.082891

  • Dröse S, Stepanova A, Galkin A (2016) Ischemic A/D transition of mitochondrial complex I and its role in ROS generation. Biochim. Biophys. Acta BBA - Bioenerg. 1857:946–957. https://doi.org/10.1016/j.bbabio.2015.12.013

    Article  CAS  Google Scholar 

  • Driedzic WR, Almeida-Val VMF (1996) Enzymes of cardiac energy metabolism in Amazonian teleosts and the fresh-water stingray (Potamotrygon hystrix). J Exp Zool 274:327–333

  • Du SNN, Mahalingam S, Borowiec BG, Scott GR (2016) Mitochondrial physiology and reactive oxygen species production are altered by hypoxia acclimation in killifish (Fundulus heteroclitus). J Exp Biol 219:1130–1138. https://doi.org/10.1242/jeb.132860

    Article  PubMed  Google Scholar 

  • Ekambaram P, Parasuraman P, Jayachandran T (2016) Differential regulation of pro- and antiapoptotic proteins in fish adipocytes during hypoxic conditions. Fish Physiol. Biochem. 42:919–934. https://doi.org/10.1007/s10695-015-0185-z

    Article  CAS  PubMed  Google Scholar 

  • Galli GLJ, Lau GY, Richards JG (2013) Beating oxygen: chronic anoxia exposure reduces mitochondrial F1FO-ATPase activity in turtle (Trachemys scripta) heart. J Exp Biol 216(17):3283–3293. https://doi.org/10.1242/jeb.087155

  • Gnaiger E, Kuznetsov AV, Schneeberger S, Seiler R, Brandacher G, Steurer W, Margreiter R (2000) Mitochondria in the cold. In: Heldmaier G, Klingenspor M. (eds) Life in the Cold. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-04162-8_45

  • Heinrichs-Caldas W, Campos DF, Paula-Silva MN, Almeida-Val VMF (2019) Oxygen-dependent distinct expression of hif-1α gene in aerobic and anaerobic tissues of the Amazon Oscar, Astronotus crassipinnis. Comp Biochem Physiol B Biochem Mol Biol 227:31–38. https://doi.org/10.1016/j.cbpb.2018.08.011

    Article  CAS  PubMed  Google Scholar 

  • Heise K, Estevez MS, Puntarulo S, Galleano M, Nikinmaa M, Pörtner HO, Abele D (2007) Effects of seasonal and latitudinal cold on oxidative stress parameters and activation of hypoxia inducible factor (HIF-1) in zoarcid fish. J Comp Physiol B 177:765–777. https://doi.org/10.1007/s00360-007-0173-4

    Article  CAS  PubMed  Google Scholar 

  • Hickey AJR, Renshaw GMC, Speers-Roesch B, Richards JG, Wang Y, Farrell AP, Brauner CJ (2012) A radical approach to beating hypoxia: depressed free radical release from heart fibres of the hypoxia-tolerant epaulette shark (Hemiscyllum ocellatum). J Comp Physiol B 182:91–100. https://doi.org/10.1007/s00360-011-0599-6

    Article  PubMed  Google Scholar 

  • Ho DH, Burggren WW (2012) Parental hypoxic exposure confers offspring hypoxia resistance in zebrafish (Danio rerio). J Exp Biol 215:4208–4216. https://doi.org/10.1242/jeb.074781

    Article  CAS  PubMed  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New York

    Google Scholar 

  • Ivanina AV, Nesmelova I, Leamy L, Sokolov EP, Sokolova IM (2016) Intermittent hypoxia leads to functional reorganization of mitochondria and affects cellular bioenergetics in marine molluscs. J Exp Biol 219(11):1659–1674. https://doi.org/10.1242/jeb.134700

  • Jiang Z-Y, Woollard ACS, Wolff SP (1991) Lipid hydroperoxide measurement by oxidation of Fe2+ in the presence of xylenol orange. Comparison with the TBA assay and an iodometric method. Lipids 26:853–856. https://doi.org/10.1007/BF02536169

    Article  CAS  PubMed  Google Scholar 

  • Johannsson OE, Giacomin M, Sadauskas-Henrique H, Campos DF, Braz-Mota S, Heinrichs-Caldas WD, Baptista R, Wood CM, Almeida-Val VMF, Val AL (2018) Does hypoxia or different rates of re-oxygenation after hypoxia induce an oxidative stress response in Cyphocharax abramoides (Kner 1858), a Characid fish of the Rio Negro? Comp Biochem Physiol A Mol Integr Physiol 224:53–67. https://doi.org/10.1016/j.cbpa.2018.05.019

    Article  CAS  PubMed  Google Scholar 

  • Junk WJ, Spare MG, Carvalho FM (1983) Distribution of fish species in a lake of the Amazon river flood plain near Manaus (lago Camaleao), with special reference o extreme oxygen conditions. Amazoniana 7:397–431

    Google Scholar 

  • Kodama K, Saydur Rahman Md, Horiguchi T, Thomas P (2012) Upregulation of hypoxia-inducible factor (HIF)-1α and HIF-2α mRNA levels in dragonet Callionymus valenciennei exposed to environmental hypoxia in Tokyo Bay. Mar Pollut Bull 64:1339–1347. https://doi.org/10.1016/j.marpolbul.2012.05.002

    Article  CAS  PubMed  Google Scholar 

  • Lau GY, Arndt S, Murphy MP, Richards JG (2019) Species- and tissue-specific differences in ROS metabolism during exposure to hypoxia and hyperoxia plus recovery in marine sculpins. J Exp Biol 222:jeb206896. https://doi.org/10.1242/jeb.206896

    Article  PubMed  Google Scholar 

  • Leveelahti L, Rytkönen KT, Renshaw GMC, Nikinmaa M (2014) Revisiting redox-active antioxidant defenses in response to hypoxic challenge in both hypoxia-tolerant and hypoxia-sensitive fish species. Fish Physiol Biochem 40:183–191. https://doi.org/10.1007/s10695-013-9835-1

    Article  CAS  PubMed  Google Scholar 

  • Lushchak VI, Bagnyukova TV (2007) Hypoxia induces oxidative stress in tissues of a goby, the rotan Perccottus glenii. Comp Biochem Physiol B Biochem Mol Biol 148:390–397. https://doi.org/10.1016/j.cbpb.2007.07.007

    Article  CAS  PubMed  Google Scholar 

  • Lushchak VI, Bagnyukova TV, Lushchak OV, Storey JM, Storey KB (2005) Hypoxia and recovery perturb free radical processes and antioxidant potential in common carp (Cyprinus carpio) tissues. Int J Biochem Cell Biol 37:1319–1330. https://doi.org/10.1016/j.biocel.2005.01.006

    Article  CAS  PubMed  Google Scholar 

  • Lushchak VI, Lushchak LP, Mota AA, Hermes-Lima M (2001) Oxidative stress and antioxidant defenses in goldfish Carassius auratus during anoxia and reoxygenation. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 280(1):R100-R107. https://doi.org/10.1152/ajpregu.2001.280.1.R100

  • Mahalingam S, McClelland GB, Scott GR (2017) Evolved changes in the intracellular distribution and physiology of muscle mitochondria in high-altitude native deer mice: Mitochondrial adaptations to high altitudes. J Physiol 595:4785–4801. https://doi.org/10.1113/JP274130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marcon JL (1996) Oxidative stress in two species of amazonian teleosts, Astronotus ocellatus and Colossoma macropomum, exposed to different oxygen tensions: a comparative approach. 148 f. Tese (Doutorado em Ecofisiologia, Ictiologia, Mamíferos aquáticos, Recursos pesqueiros, Aquacultura, Sistemática e Biol) - Instituto Nacional de Pesquisas da Amazônia, Manaus. https://bdtd.inpa.gov.br/handle/tede/1501

  • Mandic M, Regan MD (2018) Can variation among hypoxic environments explain why different fish species use different hypoxic survival strategies? J Exp Biol 221:jeb161349. https://doi.org/10.1242/jeb.161349

    Article  PubMed  Google Scholar 

  • McBryan TL, Healy TM, Haakons KL, Schulte PM (2016) Warm acclimation improves hypoxia tolerance in Fundulus heteroclitus. J Exp Biol 219:474–484. https://doi.org/10.1242/jeb.133413

    Article  PubMed  Google Scholar 

  • Mendonça FP, Magnusson WE, Zuanon J (2005) Relationships between habitat characteristics and fish assemblages in small streams of Central Amazonia. Copeia 2005:751–764 (10.1643/0045-8511(2005)005[0751:RBHCAF]2.0.CO;2Met.Biochemical adjutments to hypoxia by Amazon cichlids.pdf, n.d.)

    Article  Google Scholar 

  • Moyes CD, Mathieu-Costello OA, Brill RW, Hochachka PW (1992) Mitochondrial metabolism of cardiac and skeletal muscles from a fast (Katsuwonus pelamis) and a slow (Cyprinus carpio) fish. Can J Zool 70:1246–1253. https://doi.org/10.1139/z92-172

    Article  CAS  Google Scholar 

  • Muusze B, Marcon J, van den Thillart G, Almeida-Val V (1998) Hypoxia tolerance of Amazon fish: respirometry and energy metabolism of the cichlid Astronotus ocellatus. Comp Biochem Physiol A Mol Integr Physiol 120(1):151–156

    Article  Google Scholar 

  • Paradis S, Charles A-L, Meyer A, Lejay A, Scholey JW, Chakfé N, Zoll J, Geny B (2016) Chronology of mitochondrial and cellular events during skeletal muscle ischemiareperfusion. Am J Physiol Cell Physiol 310:C968–C982. https://doi.org/10.1152/ajpcell.00356.2015

    Article  PubMed  PubMed Central  Google Scholar 

  • Pazin FV, Magnusson WE, Zuanon J, Mendonça FP (2006) Fish assemblages in temporary ponds adjacent to ‘terra-firme’ streams in Central Amazonia. Freshw Biol 51:1025–1037

    Article  Google Scholar 

  • Price TD, Qvarnström A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc R Soc Lond Ser B Biol Sci 270(1523):1433–1440

  • Regan MD, Mandic M, Dhillon RS, Lau GY, Farrell AP, Schulte PM, Seibel BA, Speers-Roesch B, Ultsch GR, Richards JG (2019) Don’t throw the fish out with the respirometry water. J Exp Biol 222:200253. https://doi.org/10.1242/jeb.200253

    Article  Google Scholar 

  • Rolf DF, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77(3):731–58. https://doi.org/10.1152/physrev.1997.77.3.731

    Article  Google Scholar 

  • Sabino J, Zuanon JAS (1998) A stream fish assemblage in Central Amazonia: distribution, activity patterns and feeding behavior. Ichthyol Explor Fresh 8(3):201–210

    Google Scholar 

  • Saint-Paul U (1984) Physiological adaptation to hypoxia of a neotropical characoid fish Colossoma macropomum, Serrasalmidae. Environ Biol Fishes 11:53–62. https://doi.org/10.1007/BF00001845

  • Sappal R, Fast M, Purcell S, MacDonald N, Stevens D, Kibenge F, Siah A, Kamunde,C (2016) Copper and hypoxia modulate transcriptional and mitochondrial functionalbiochemical responses in warm acclimated rainbow trout (Oncorhynchus mykiss). Environmental Pollution 211:291–306. https://doi.org/10.1016/j.envpol.2015.11.050

  • Sokolova IM, Sokolov EP, Haider F (2019) Mitochondrial mechanisms underlying tolerance to fluctuating oxygen conditions: lessons from hypoxia-tolerant organisms. Integr Comp Biol 59:938–952. https://doi.org/10.1093/icb/icz047

  • Solaini G, Baracca A, Lenaz G, Sgarbi G (2010) Hypoxia and mitochondrial oxidative metabolism. Biochim Biophys Acta Bioenerg 1797:1171–1177. https://doi.org/10.1016/j.bbabio.2010.02.011

    Article  CAS  Google Scholar 

  • Sloman KA, Wood CM, Scott GR, Wood S, Kajimura M, Johannsson OE, ... Val AL (2006) Tribute to RG Boutilier: the effect of size on the physiological and behavioural responses of oscar, Astronotus ocellatus, to hypoxia. J Exp Biol 209(7):1197–1205

  • Steffensen J (1989) Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiol. Biochem 6:49–59

  • Thomas P, Rahman MdS, Khan IA, Kummer JA (2007) Widespread endocrine disruption and reproductive impairment in an estuarine fish population exposed to seasonal hypoxia. Proc R Soc B Biol Sci 274:2693–2702. https://doi.org/10.1098/rspb.2007.0921

    Article  CAS  Google Scholar 

  • Turrens JF (1997) Superoxide production by the mitochondrial respiratory chain.Bioscience Reports 17(1):3–8. https://doi.org/10.1007/978-1-4614-3573-0_6

  • Val AL, Almeida-Val VMF (1996) Fishes of the Amazon and their environment: physiological and biochemical aspects, Zoophysiology. Vol. 32. Springer-Verlag, Berlin, Heidelberg

    Google Scholar 

  • Val AL, Almeida-Val VMF, Paula-Silva MN (1998) Hypoxia adaptation in fish of the Amazon: a never-ending task. S Afr J Zool 33:107–114

    Google Scholar 

  • Val AL, Almeida-Val VMF (1996) Fishes of the Amazon and their environment: Physiological and biochemical aspects. In: Zoophysiology. vol. 32 Springer-Verlag, Berlin, Heidelberg

  • van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149. https://doi.org/10.1016/S1382-6689(02)00126-6

    Article  PubMed  Google Scholar 

  • Víg É, Nemcsók J (1989) The effects of hypoxia and paraquat on the superoxide dismutase activity in different organs of carp, Cyprinus carpio L. J Fish Biol 35:23–25. https://doi.org/10.1111/j.1095-8649.1989.tb03389.x

    Article  Google Scholar 

  • Woo S, Denis V, Won H, Shin K, Lee G, Lee T-K, Yum S (2013) Expressions of oxidative stress-related genes and antioxidant enzyme activities in Mytilus galloprovincialis (Bivalvia, Mollusca) exposed to hypoxia. Zool. Stud. 52:15. https://doi.org/10.1186/1810-522X-52-15

    Article  CAS  Google Scholar 

  • Wood CM (2018) The fallacy of the P crit – are there more useful alternatives? J. Exp. Biol. 221:jeb163717. https://doi.org/10.1242/jeb.163717

    Article  PubMed  Google Scholar 

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Acknowledgements

We also thank Dr. Adalberto Luis Val for his valuable contributions with suggestions and discussions to this work.

Funding

This study was funded by the Brazilian National Research Council (CNPq, process N465540/2014-7), Coordination for the Improvement of Higher Education Personel (CAPES, finance code 001) Amazonas State Research Foundation (FAPEAM, process 062.01187/2017) that supported INCT/ADAPTA. WHC was the recipient of a doctoral fellowship from CNPq and VMFAV is the recipient of a CNPq research fellowship.

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  1. LEEM – Laboratório de Ecofisiologia e Evolução Molecular, Instituto Nacional de Pesquisas da Amazônia, Campus I, Manaus, Amazonas, Brazil

    Waldir Heinrichs-Caldas & Vera Maria Fonseca de Almeida-Val

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  1. Waldir Heinrichs-Caldas
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Both authors, Waldir Heinrichs-Caldas and Vera Maria Fonseca de Almeida-Val, contributed equally for the manuscript.

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Correspondence to Waldir Heinrichs-Caldas.

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Heinrichs-Caldas, W., de Almeida-Val, V.M.F. Hypoxia tolerance in two amazon cichlids: mitochondrial respiration and cellular metabolism adjustments are result of species environmental preferences and distribution. Fish Physiol Biochem 47, 1759–1775 (2021). https://doi.org/10.1007/s10695-021-01000-0

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