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Functional characterization of the oxidative capacity of mitochondria and glycolytic assessment in benthic aquatic organisms

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Abstract

The metabolism of benthic aquatic invertebrates, populating transitional water ecosystems, is influenced by both physiological and environmental factors, thus involving an adjustment of physiological processes which has a metabolic cost. In order to discover changes in metabolic pathways in response to specific factors, it’s firstly necessary characterizing the principal cellular metabolic activities of the small benthic aquatic organisms. We approach here the bioenergetic state issue of two benthic organisms, i.e. Lekanesphaera monodi and Gammarus insensibilis, evidencing that no apparent and statistically significative differences between them in aerobic as well in glycolytic capacities are detected, except for COX activity.

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Abbreviations

AA:

Antimycin A

ADK:

Adenylate kinase

ANT:

Adenine nucleotide translocator

Ap5A:

P1,P5-Di(adenosine-5′)penta-phosphate

ASC:

Ascorbate

ATP D.S.:

ATP detecting system

ATR:

Atractyloside

β-OH:

β−hydroxybutyrate

CN− :

Potassium cyanide

COX:

Cytochrome oxidase

CS:

Citrate synthase

GDH:

Glutamate dehydrogenase

HK:

Hexokinase

LDH:

Lactate dehydrogenase

NaN3 :

Sodium azide

OLIGO:

Oligomycin

PBS:

Phosphate buffer saline medium

PFK:

Phosphofructokinase

PK:

Pyruvate kinase

RAM:

Rotenone plus antimycin A plus mixothiazole

RCI:

Respiratory control index

ROT:

Rotenone

S.D.:

Standard deviation

SUCC:

Succinate

TMPD:

N,N,N′,N′-tetramethyl-p-phenylenediamine dihydrochloride

References

  • Ahmad A, Ahmad S, Schneider BK, Allen CB, Chang LY, White CW (2002) Elevated expression of hexokinase II protects human lung epithelial-like A549 cells against oxidative injury. Am J Physiol Lung Cell Mol Physiol 283:L573–L584

    Article  CAS  Google Scholar 

  • Allan EL, Froneman PW, Hodgson AN (2006) Effects of temperature and salinity on the standard metabolic rate (SMR) of the caridean shrimp Palaemon peringueyi. J Exp Mar Biol Ecol 337:103–108

    Article  CAS  Google Scholar 

  • Atlante A, Passarella S, Quagliariello E, Moreno G, Salet C (1989) Haematoporphyrin derivative (Photofrin II) photosensitization of isolated mitochondria: inhibition of ADP/ATP translocator. J Photochem Photobiol B 4:35–46

    Article  CAS  Google Scholar 

  • Atlante A, Giannattasio S, Bobba A, Gagliardi S, Petragallo V, Calissano P, Marra E, Passarella S (2005) An increase in the ATP levels occurs in cerebellar granule cells en route to apoptosis in which ATP derives from both oxidative phosphorylation and anaerobic glycolysis. Biochim Biophys Acta 1708:50–62

    Article  CAS  Google Scholar 

  • Atlante A, Bobba A, de Bari L, Fontana F, Calissano P, Marra E, Passarella S (2006) Caspase-dependent alteration of the ADP/ATP translocator triggers the mitochondrial permeability transition which is not required for the low-potassium-dependent apoptosis of cerebellar granule cells. J Neurochem 97:1166–1181

    Article  CAS  Google Scholar 

  • Atlante A, de Bari L, Bobba A, Marra E, Passarella S (2007) Transport and metabolism of L-lactate occur in mitochondria from cerebellar granule ce lls and are modified in cells undergoing low potassium dependent apoptosis. Biochim Biophys Acta 1767:1285–1299

    Article  CAS  Google Scholar 

  • Atlante A, Amadoro G, Bobba A, de Bari L, Corsetti V, Pappalardo G, Marra E, Calissano P, Passarella S (2008) A peptide containing residues 26–44 of tau protein impairs mitochondrial oxidative phosphorylation acting at the level of the adenine nucleotide translocator. Biochim Biophys Acta 1777:1289–1300

    Article  CAS  Google Scholar 

  • Atlante A, Seccia TM, Marra E, Passarella S (2011) The rate of ATP export in the extramitochondrial phase via the adenine nucleotide translocator changes in aging in mitochondria isolated from heart left ventricle of either normotensive or spontaneously hypertensive rats. Mech Ageing Dev 132:488–495

    Article  CAS  Google Scholar 

  • Bénit P, Goncalves S, Philippe Dassa E, Brière JJ, Martin G, Rustin P (2006) Three spectrophotometric assays for the measurement of the five respiratory chain complexes in minuscule biological samples. Clin Chim Acta 374:81–86

    Article  Google Scholar 

  • Bobba A, Amadoro G, Valenti D, Corsetti V, Lassandro R, Atlante A (2013) Mitochondrial respiratory chain Complexes I and IV are impaired by beta-amyloid via direct interaction and through Complex I-dependent ROS production, respectively. Mitochondrion 13:298–311

    Article  CAS  Google Scholar 

  • Bobba A, Amadoro G, La Piana G, Calissano P, Atlante A (2015) Glycolytic enzyme upregulation and numbness of mitochondrial activity characterize the early phase of apoptosis in cerebellar granule cells. Apoptosis 20:10–28

    Article  CAS  Google Scholar 

  • Cognetti G, Maltagliati F (2008) Perspectives on the ecological assessment of transitional waters. Mar Pollut Bull 56:607–608

    Article  CAS  Google Scholar 

  • D’Erchia AM, Atlante A, Gadaleta G, Pavesi G, Chiara M, De Virgilio C, Manzari C, Mastropasqua F, Prazzoli GM, Picardi E, Gissi C, Horner D, Reyes A, Sbisà E, Tullo A, Pesole G (2015) Tissue-specific mtDNA abundance from exome data and its correlation with mitochondrial transcription, mass and respiratory activity. Mitochondrion 20:13–21

    Article  Google Scholar 

  • Draxl A, Eigentler A, Gnaiger E (2013) PBI-Shredder HRR-Set: preparation of tissue homogenates for diagnosis of mitochondrial respiratory function. Mitochondrial Physiol Netw 17:1–8

    Google Scholar 

  • Fonyó A, Vignais PV (1979) Phosphate retention and release during ATP hydrolysis in liver mitochondria. FEBS Lett 102:301–305

    Article  Google Scholar 

  • Hoback WW, Barnhart MC (1996) Lethal limits and sublethal effects of hypoxia on the amphipod Gammarus pseudolimnaeus. J N Am Benthol Soc 15:117–126

    Article  Google Scholar 

  • Kunz WS (2003) Different metabolic properties of mitochondrial oxidative phosphorylation in different cell types--important implications for mitochondrial cytopathies. Exp Physiol 88:149–154

    Article  CAS  Google Scholar 

  • Lampert W (1984) The measurement of respiration. In: Downing JA, Rigler FH (eds) A manual on methods for the assessment of secondary productivity in fresh water. Blackwell Scientific Publications, Oxford, pp 413–469

    Google Scholar 

  • Leary SC, Battersby BJ, Moyes CD (1998) Inter-tissue differences in mitochondrial enzyme activity, RNA and DNA in rainbow trout (Oncorhynchus mykiss). J Exp Biol 201:3377–3384

    CAS  Google Scholar 

  • Leverve XM, Fontaine E (2001) Role of substrates in the regulation of mitochondrial function in situ. IUBMB Life 52:221–229, Review

    Article  CAS  Google Scholar 

  • Lubec B, Chiappe-Gutierrez M, Hoeger H, Kitzmueller E, Lubec G (2000) Glucose transporters, hexokinase, and phosphofructokinase in brain of rats with perinatal asphyxia. Pediatr Res 47:84–88

    Article  CAS  Google Scholar 

  • MacArthur RH, Levins R (1964) Competition, habitat selection, and character displacement. Proc Natl Acad Sci U S A 51:1207–1210

    Article  CAS  Google Scholar 

  • MacDonald MJ (1989) Does glyceraldehyde enter pancreatic islet metabolism via both the triokinase and the glyceraldehyde phosphate dehydrogenase reactions? A study of these enzymes in islets. Arch Biochem Biophys 270:15–22

    Article  CAS  Google Scholar 

  • Millet B, Guelorget O (1994) Spatial and seasonal variability in the relationships between benthic communities and physical environment in a lagoon ecosystem Mar Ecol Prog Ser 161–174

  • Mills EL (1969) The community concept in marine zoology, with comments on continua and instability in some marine communities: a review. J Fish Res Board Can 26:1415–1428

    Article  Google Scholar 

  • Mitton JB, Carey C, Kocher TD (1986) The relation of enzyme heterozygosity to standard and active oxygen-consumption and body size of tiger salamanders, Ambystoma tigrinum. Physiol Zool 59:574–582

    Article  CAS  Google Scholar 

  • Occhipinti-Ambrogi A, Forni G (2004) Applicazione di indici biotici basati sulle comunità macrobentoniche di fondi incoerenti per la valutazione della qualità ambientale. Biol Mar Medit 11:93–100

    Google Scholar 

  • Ostuni A, Passarella S, Quagliariello E (1993) Photomodulation of glutamate dehydrogenase properties by red light. J Photochem Photobiol B 20:101–111

    Article  CAS  Google Scholar 

  • Passarella S, Atlante A, Valenti D, de Bari L (2003) The role of mitochondrial transport in energy metabolism. Mitochondrion 2:319–343

    Article  CAS  Google Scholar 

  • Paul JF, Scott KJ, Campbell DE, Gentile JH, Strobel CS, Valente RM, Weisberg SB, Holland AF, Ranasinghe JA (2001) Developing and applying a benthic index of estuarine condition for the Virginian biogeographic province. Ecol Indic 1:83–99

    Article  Google Scholar 

  • Pesole G (2008) What is a gene? An updated operational definition. Gene 417:1–4

    Article  CAS  Google Scholar 

  • Pfeiffer T, Schuster S, Bonhoeffer S (2001) Cooperation and competition in the evolution of ATP-producing pathways. Science 292:504–507

    Article  CAS  Google Scholar 

  • Pizzuto R, Paventi G, Atlante A, Passarella S (2010) Pyruvate kinase in pig liver mitochondria. Arch Biochem Biophys 495:42–48

    Article  CAS  Google Scholar 

  • Pujolar JM, Maes GE, Vancoillie C, Volckaert FAM (2005) Growth rate correlates to individual heterozygosity in the european eel, Anguilla anguilla L. Evolution 59:189–199

    CAS  Google Scholar 

  • Robinson JB Jr, Srere PA (1985) Organization of Krebs tricarboxylic acid cycle enzymes in mitochondria. J Biol Chem 260:10800–10805

    CAS  Google Scholar 

  • Salomon M, Buchholz F (2000) Effects of temperature on the respiration rates and the kinects of citrate synthase in two species of Idotea (Isopoda, Crustacea). Comp Biochem Phys B 125:71–81

    Article  CAS  Google Scholar 

  • Seccia TM, Atlante A, Vulpis V, Marra E, Passarella S, Pirrelli A (1998) Mitochondrial energy metabolism in the left ventricular tissue of spontaneously hypertensive rats: abnormalities in both adeninenucleotide and phosphate translocators and enzyme adenylate-kinase and creatine-phosphokinase activities. Clin Exp Hypertens 20:345–358

    Article  CAS  Google Scholar 

  • Teska WR, Smith MH, Novak JM (1990) Food quality, heterozygosity and fitness correlates in Peromyscus polionotus. Evolution 44:1318–1325

    Article  Google Scholar 

  • Turelli M, Barton NH, Coyne JA (2001) Theory and speciation. Trends Ecol Evol 16:330–343

    Article  Google Scholar 

  • Vignes F, Fedele M, Pinna M, Mancinelli G, Basset A (2012) Variability of Lekanesphaera monodi metabolic rates with habitat trophic status. Acta Oecol 41:58–64

    Article  Google Scholar 

  • Waddell WJ, Hill C (1956) A simple ultraviolet spectrophotometric method for the determination of protein. J Lab Clin Med 48:311–314

    CAS  Google Scholar 

  • Wanders RJ, Van Roermund CW, Meijer AJ (1984) Analysis of the control of citrulline synthesis in isolated rat-liver mitochondria. Eur J Biochem 142:247–254

    Article  CAS  Google Scholar 

  • Weisberg SB, Ranasinghe JA, Dauer DM, Schaffner LC, Diaz RJ, Frithsen JB (1997) An estuarine benthic index of biotic integrity (B-BI) for Chesapeake Bay. Estuaries 20:149–158

    Article  Google Scholar 

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Authors and Affiliations

  1. Institute of Biomembrane and Bioenergetics, CNR, Via G. Amendola 165/A, 70126, Bari, Italy

    A. Atlante & A. Bobba

  2. Department of Biological and Environmental Sciences & Technologies, University of Salento, Lecce, Italy

    A. Basset & F. Vignes

  3. Institute of Cristallography, CNR, Bari, Italy

    R. Lassandro

  4. Department of Biology, University of Bari, Bari, Italy

    F. Mastrototaro

Authors
  1. A. Atlante
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  2. A. Basset
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  3. A. Bobba
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  4. R. Lassandro
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  5. F. Mastrototaro
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  6. F. Vignes
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Correspondence to A. Atlante.

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Atlante, A., Basset, A., Bobba, A. et al. Functional characterization of the oxidative capacity of mitochondria and glycolytic assessment in benthic aquatic organisms. J Bioenerg Biomembr 48, 249–257 (2016). https://doi.org/10.1007/s10863-016-9647-y

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  • DOI: https://doi.org/10.1007/s10863-016-9647-y

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