BEC 2020.1 doi10.26124bec2020-0001.v1

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Mitochondrial physiology

Has title::Gnaiger E et al ― MitoEAGLE Task Group (2020) Mitochondrial physiology. Bioenerg Commun 2020.1. https://doi.org/10.26124/bec:2020-0001.v1

» [[Has info::Bioenerg Commun 2020.1. published online 2020-05-20

]]

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Abstract: [[has abstract:: doi:10.26124/bec:2020-0001.v1

Versions (v1) 2020-05-20 - »Link to all versions«

As the knowledge base and importance of mitochondrial physiology to evolution, health and disease expands, the necessity for harmonizing the terminology concerning mitochondrial respiratory states and rates has become increasingly apparent. The chemiosmotic theory establishes the mechanism of energy transformation and coupling in oxidative phosphorylation. The unifying concept of the protonmotive force provides the framework for developing a consistent theoretical foundation of mitochondrial physiology and bioenergetics. We follow the latest SI guidelines and those of the International Union of Pure and Applied Chemistry (IUPAC) on terminology in physical chemistry, extended by considerations of open systems and thermodynamics of irreversible processes. The concept-driven constructive terminology incorporates the meaning of each quantity and aligns concepts and symbols with the nomenclature of classical bioenergetics. We endeavour to provide a balanced view of mitochondrial respiratory control and a critical discussion on reporting data of mitochondrial respiration in terms of metabolic flows and fluxes. Uniform standards for evaluation of respiratory states and rates will ultimately contribute to reproducibility between laboratories and thus support the development of data repositories of mitochondrial respiratory function in species, tissues, and cells. Clarity of concept and consistency of nomenclature facilitate effective transdisciplinary communication, education, and ultimately further discovery.]]

• Bioblast editor: [[has editor::Gnaiger E]]

Keywords—MitoPedia

• Cell count • Coupling-control ratio • Electron transfer pathway • Flow • Flux • Flux control ratio • IUPAC • LEAK respiration • Mitochondrial marker • Mitochondrial preparations • Respiratory states • Normalization of rate • Oxidative phosphorylation • Oxygen • Phosphorylation efficiency • Protonmotive force • Residual oxygen consumption • SI - The International System of Units • Uncoupling

Keywords—MitoPedia - >>>>>>> - Click on [Expand] or [Collapse] - >>>>>>>

Keywords—MitoPedia, including Table 8. Terms, symbols, and units. SI base units are used, except for the liter [L = dm³]. SI refers to ref. [11].

Term	Link to MitoPedia term	Symbol	Unit	Links and comments
adenosine diphosphate	ADP	ADP	-	Tab. 1; Fig. 1, 2, 5
adenosine monophosphate	AMP	AMP	-	2 ADP ↔ ATP+AMP
adenosine triphosphate	ATP	ATP	-	Fig. 2, 5
adenylates	Adenine nucleotides	AMP, ADP, ATP	-	Section 2.5.1
alternative quinol oxidase	Alternative oxidase	AOX	-	Fig. 1B
amount of substance B	Amount	nB or n(B)	[mol]	SI; amount nB of B versus count NB of B
ATP yield per O2	ATP yield	YP»/O2	1	P»/O2 ratio measured in any respiratory state
catabolic rate of respiration	Cell respiration	JkO2; IkO2	varies	Fig. 1, 3; flux J versus flow I
catabolic reaction	Cell respiration	k	-	Fig. 1, 3
cell count	Count	Nce	[x]	Tab. 4; Fig. 5; see number of cells; countable object s=ce
cell-count concentration	Concentration	Cce	[x∙L­-1]	Tab. 4; Cce = Nce∙V-1; count concentration C versus amount concentration c; subscript ce indicates the entity type: concentration of ce. But it does not signal 'per entity', which would be written as 'per cell' Xce.
cell mass	Body mass	mce	[kg]	Tab. 5; Fig. 5; mass of cells m versus mass per cell (per single entity cell) MXce
cell mass, mass per cell	Body mass	MXce	[kg∙x­-1]	Tab. 5; Fig. 5; mass per single cell MXce; upper case M and subscript X signal 'per count', subscript ce signals the entity s=ce; in a context restricted to cells or molecules or a particular organism such as humans, the abbreviated symbol M [kg∙x­-1] provides a sufficiently informative signal, particularly in combination with the explicit unit.
cell-mass concentration in chamber	Concentration	Cmce	[kg∙L­-1]	see Cms: Tab. 4; Cmce = mce∙V-1; upper case C alone would signal 'count concentration' (CN is more explicit), whereas the signal for 'mass concentration' is in the combination Cm.
cell viability index	Cell viability	VI	-	VI = Nvce∙Nce­-1 = 1 - Ndce∙Nce­-1
charge number per entity XB	Charge number	zB	1	zB = QB·e-1 (IUPAC); Tab. 6; zO2 = = QO2·e-1 = 4; IUPAC uses the term 'charge number of an ion' which should be changed to 'charge number per ion', or more clearly to 'charge number per ion number'. The symbol z carries the message 'number of elementary charges per number', and the subscript carries the message on the type of entity X.
Complexes I to IV	Complex I	CI to CIV	-	respiratory ET Complexes are redox proton pumps; Fig. 1B; F1FO-ATPase is not a redox proton pump of the ETS, hence the term CV is not recommended
concentration of B, amount	Concentration	cB = NB∙V­-1	[mol∙L­-1]	SI: amount of substance concentration Cohen 2008 IUPAC Green Book; the molar and count formats are distinguished as nB and NB, respectively.
concentration of O2, amount	Concentration	cO2 = nO2∙V­-1	[mol∙L­-1]	Box 2; [O2]
concentration of s, count	Concentration	Cs = Ns∙V­-1	[x∙L-1] Tab. 4 (number concentration Cohen 2008 IUPAC Green Book); the signal for count concentration is given by the upper case C in contrast to c for amount concentration. In both cases, the subscript X indicates the entity type, not to be confused with a number of entities.
count format	Format	N	[x]	Tab. 4, 5; Fig. 5
count of Xs	Count	Ns	[x]	SI; see number of entities Xs
coupling control	Coupling-control ratio	CCR	-	Section 2.4.1
coupling control state	Coupling control state	CCS	-	Section 2.4.1
dead cells	Cell viability	dce	-	Tab. 5
electrical format	Format	e	[C]	Tab. 6
electron transfer pathway	Electron transfer pathway	ET pathway	-	Overview; Fig. 1
electron transfer, state	Electron transfer pathway	ET	-	Tab. 1; Fig. 2B, 4 (State 3u)
electron transfer system	Electron transfer pathway	ETS	-	Fig. 2B, 4 (electron transport chain)
elementary entity	Entity	Xs	[x]	single countable object of sample type s; Tab. 4
ET capacity	ET capacity	E	varies	rate; Tab. 1; Fig. 2
ET-excess capacity	ET capacity	E-P	varies	Fig. 2
flow, for O2	Flow	IO2	[mol∙s-­1]	system-related extensive quantity; Fig. 5
flux, for O2	Flux	JO2	varies	size-specific quantity; Fig. 5
flux control ratio	Flux control ratio	FCR	1	background/reference flux; Fig. 5
hyphenation	Hyphenation	-	-	Updates in comparison to Gnaiger 2019 MitoFit Preprints
inorganic phosphate	Phosphate	Pi	-	Fig. 1C
inorganic phosphate carrier	Phosphate carrier	PiC	-	Fig. 1C
International Union of Pure and Applied Chemistry, IUPAC	IUPAC	IUPAC	-	Cohen 2008 IUPAC Green Book
International System of Units	International System of Units	SI	-	Cohen 2008 IUPAC Green Book
isolated mitochondria	Isolated mitochondria	imt	-	[11]
LEAK state	LEAK respiration	LEAK	-	Tab. 1; Fig. 2 (compare State 4)
LEAK respiration	LEAK respiration	L	varies	rate; Tab. 1; Fig. 2
living cells	Living cells	ce	-	Tab. 5 (intact cells)
mass, dry mass	Body mass	md	[kg]	Fig. 5 (dry weight)
mass, wet mass	Body mass	mw	[kg]	Fig. 5 (wet weight)
mass concentration of sample s in chamber	Concentration	Cms	[kg∙L-1]	Tab. 4
mass format	Format	m	[kg]	Tab. 4
mass of sample s in a mixture	Mass	ms	[kg]	SI: mass of pure sample mS
mass per single object	Body mass	MNX	[kg∙x­1]	Fig. 5; Tab. 4; SI: m(X); compare molar mass M(X)
MITOCARTA	MITOCARTA
mitochondria or mitochondrial	Mitochondria	mt	-	Box 1
mitochondrial concentration	Mitochondrial marker, Concentration	CmtE = mtE∙V-1	[mtEU∙L-1]	Tab. 4
mitochondrial content per X	Mitochondrial marker	mtENX	[mtEU∙x­-1]	mtENX = mtE∙NX-1; Tab. 4
mitochondrial density per ms	Mitochondrial marker, Density	DmtE/ms	[mtEU∙kg­-1]	DmtE/ms=mtE∙ms-1; Tab. 4
mitochondrial density per Vs	Mitochondrial marker, Density	DmtE/Vs	[mtEU∙kg­-1]	DmtE/Vs=mtE∙Vs-1; Tab. 4
mitochondrial DNA	Mitochondria	mtDNA	-	Box 1
mitochondrial elementary marker	Mitochondria	mtE	[mtEU]	quantity of mt-marker; Tab. 4
mitochondrial elementary unit	Mitochondria	mtEU	varies	specific units for mt-marker; Tab. 4
mitochondrial inner membrane	Mitochondrial inner membrane	mtIM	-	Fig. 1; Box 1 (MIM)
mitochondrial outer membrane	Mitochondrial outer membrane	mtOM	-	Fig. 1; Box 1 (MIM)
mitochondrial preparations	Mitochondrial preparations	mt-prep	-	Tab. 5
mitochondrial recovery	Mitochondrial recovery	YmtE	1	fraction of mtE recovered from the tissue sample in imt-stock
mitochondrial yield	Mitochondrial yield	YmtE/ms	[mtEU∙kg-1]	mt-yield in imt-stock per mass of tissue sample; YmtE/ms=YmtE∙DmtE
MitoPedia	MitoPedia, MitoPedia: Respiratory states
molar format	Format	n	[mol]	Tab. 6
molar mass	Molar mass	MB	[kg∙mol-1]	compare MNB [kg∙x-1]; SI M(X)
negative	Protonmotive force	neg	-	Fig. 4
normalization of rate	Normalization of rate	-	-	Tab. 4; Fig. 5
number of cells	Count	Nce	[x]	total cell count of living cells, Nce = Nvce + Ndce; Tab. 4, 5
number of dead cells	Cell viability	Ndce	[x]	non-viable cell count, loss of plasma membrane barrier function; Tab. 5
number of entities B	Count	NB	[x]	Tab. 4 Cohen 2008 IUPAC Green Book
number of entities X; count	Count	NX	[x]	‘count’ is an SI quantity [11], but the counting unit [x] is not in the SI [95]; Tab. 4; Fig. 5
number of viable cells	Cell viability	Nvce	[x]	viable cell count, intact plasma membrane barrier function; Tab. 5
organisms	Organism	org	-	Tab. 5
oxidative phosphorylation	Oxidative phosphorylation	OXPHOS	-	Tab. 1
OXPHOS-capacity	OXPHOS-capacity	P	varies	rate; Tab. 1; Fig. 2
OXPHOS state	OXPHOS-capacity	OXPHOS	-	Tab. 1; Fig. 2; OXPHOS-state distinguished from the process OXPHOS (State 3 at kinetically-saturating [ADP] and [Pi])
oxygen concentration	Oxygen concentration	cO2 = nO2∙V­-1	[mol∙L­-1]	[O2]; Section 3.2
oxygen solubility	Oxygen solubility	SO2	[µmol·kPa-1]	Section 2.6.3
oxygen flux, in reaction r	Oxygen flux	JrO2	varies	Overview
pathway control state	Pathway control state	PCS	-	Section 2.2
permeability transition	Permeability transition	mtPT	-	Fig. 3; Section 2.4.3 (MPT)
permeabilized cells	Permeabilized cells	pce	-	experimental permeabilization of plasma membrane; Tab. 5
permeabilized muscle fibers	Permeabilized muscle fibers	pfi	-	Tab. 5
permeabilized tissue	Permeabilized tissue	pti	-	Tab. 5
phosphorylation of ADP to ATP	Oxidative phosphorylation	P»	-	Tab. 1, 2; Fig. 1, 4
phosphorylation efficiency	Ergodynamic efficiency	ε	1	Section 2.4.1
P»/O2 ratio	Oxidative phosphorylation	P»/O2	1	mechanistic YP»/O2, calculated from pump stoichiometries; Fig. 1c
positive	positive	Protonmotive force	-	Fig. 4
proton in the neg compartment	Protonmotive force	H+neg	[x]	Fig. 4
proton in the pos compartment	proton in the positive compartment	H+pos	[x]	Fig. 4
protonmotive force	protonmotive force	pmF	[V]	Overview; Tab. 1; Fig 1a, 2, 4
publication efficiency	publication efficiency			Harmonization of nomenclature; Executive summary
quantities, symbols, and units	Quantities, symbols, and units	-	-	An explanation of symbols and unit [x]
rate in ET state	Electron transfer pathway	E	varies	ET capacity; Tab. 1; Fig. 2, 4
rate in LEAK state	LEAK respiration	L	varies	Tab. 1: L(n), L(T), L(Omy); Fig. 2, 4
rate in OXPHOS-state	OXPHOS-capacity	P	varies	OXPHOS-capacity; Tab.1; Fig. 2, 4
rate in ROX state	Residual oxygen consumption	Rox	varies	Overview; Tab. 1
residual oxygen consumption	Residual oxygen consumption	ROX; Rox	-	state ROX; rate Rox; Tab. 1
respiration	Respirometry	JrO2	varies	rate of reaction r; Overview
respiratory state	MitoPedia: Respiratory states	-	-	Tab. 1, 3; Fig. 2, 4
respiratory supercomplex	Supercomplex	SCInIIInIVn	-	supramolecular assemblies with variable copy numbers (n) of CI, CIII and CIV; Box 1
sample in a mixture	Sample	s	-	diluted sample; Tab. 4, 5
steay state	Steady state	-	-	Section 2.5.6
substrate concentration at half-maximal rate	Concentration	c50	[mol∙L­-1]	Section 2.1.2
substrate-uncoupler-inhibitor-titration	Substrate-uncoupler-inhibitor titration	SUIT	-	Section 2.2
system	System	-	-	Fig. 5
tissue homogenate	Tissue homogenate	thom	-	Tab. 5
unit elementary entity	Entity	UX	[x]	single countable object; Tab. 4, 5
uncoupling	Uncoupler titrations	-	-	Tab 2; Fig. 3
viable cells	Viable cells	vce	-	Tab. 5
volume format	Format	V	[L]	Tab. 6
volume of experimental chamber	Volume	V	[L]	liquid volume V including the sample s; Tab. 4, 7; Fig. 5
volume of sample s in a mixture	Volume	Vs	[L]	Tab. 5; Fig. 5

Authors: MitoEAGLE Task Group

• Corresponding author

Erich Gnaiger

Chair COST Action CA15203 MitoEAGLE

T +43 512 566796 15, F +43 512 566796 20

[email protected] | www.mitoeagle.org

• Coauthors (listed in alphabetical order); number of coauthors: 666

• Affiliations: click on the hyperlinks (author names) to open the person pages with affiliations and addresses.
• Many coauthors have made significant additions and suggestions for improvement of the manuscript. All coauthors confirm to have read the final manuscript, and to agree to implement or discuss the recommendations in future manuscripts, presentations and teaching materials.

• Copyright: © 2020 The Authors

This is an Open Access BEC article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited. © remains with the authors, who have granted Bioenergetics Communications an Open Access publication licence in perpetuity.

Acknowledgements

• We thank Marija Beno for management assistance, and Peter R Rich for valuable discussions. This publication is based upon work from COST Action CA15203 MitoEAGLE, supported by COST (European Cooperation in Science and Technology), in cooperation with COST Actions CA16225 EU-CARDIOPROTECTION and CA17129 CardioRNA; K-Regio project MitoFit funded by the Tyrolian Government, and project NextGen-O2k which has received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement No. 859770 and partially funded printing and international dissemination of the publication.
• Several investigators were funded by Short-Term Scientific Missions MitoEAGLE.
• Authors were funded by their individual projects.

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Overview. Internal and external respiration. (mt) Mitochondrial catabolic respiration J_kO2 is the O₂ consumption in the oxidation of fuel substrates (electron donors) and reduction of O₂ catalysed by the electron transfer system ETS, which drives the protonmotive force pmF. J_kO2 excludes mitochondrial residual oxygen consumption, mt-Rox.

Discussion — updates — versions

On a Comment in Nature Metabolism

Gnaiger Erich 2020-07-28

One month ago one of our coauthors (Pablo M Garcia-Roves) sent me the reference to a Comment on metabolic terminology published on 2020-05-15 in Nature Metabolism. The present Bioenergetics Communication is deeply concerned about terminology and communication of concepts. Control and regulation (Section 2.7) is profoundly covered in a contribution by coauthor David Fell (our ref [43]). My expertise in thermodynamics (as a former member of an IUPAC Steering Committee; see also ref [50]) motivated me to the statement: "Thus mitochondria are elementary components of energy transformation. Energy is a conserved quantity and cannot be lost or produced in any internal process (First Law of Thermodynamics). Open and closed systems can gain or lose energy only by external fluxes—by exchange with the environment. Therefore, energy can neither be produced by mitochondria, nor is there any internal process without energy conservation (page 12, Section 2.4.1. Coupling).

In the Nature Metabolism Comment, some statements on control and regulation are followed by: "More striking are the frequently made statements that mitochondria ‘create’ or ‘produce’ energy, which are fundamentally incorrect, given that energy can neither be created or destroyed (according to the first law of thermodynamics)" (Nature Metabolism 2, June 2020, p 476). The two authors of this Comment are not known for covering thermodynamics in their publication record, although this is not really needed for such a general statement. What is more interesting are the following coincidences, which cannot be interpreted due to lack of a statistically relevant sample of observations.

1. One of the 'Comment'-authors joined as a coauthor of the MitoEAGLE manuscript 'States and rates' after Version 2018-10-17(44), which included already our comment on energy conservation.
2. The preprint Version 6 (Gnaiger E, Aasander Frostner E, Abdul Karim N, Abdel-Rahman EA, Abumrad NA, Acuna-Castroviejo D, Adiele RC, et al (2019) Mitochondrial respiratory states and rates. MitoFit Preprint Arch doi:10.26124/mitofit:190001.v6) was the basis of manuscript submission to Nature Metabolism already last year.
3. The preprint was not cited by the 'Comment'-authors, despite quite obvious overlap of concerns on terminology. If one of our coauthors claims, that she was not aware of the contents in the preprint 'States and rates' (now the present BEC 'Mitochondrial physiology'), this should be an issue of questioning coauthorship in the BEC paper.
4. Is there any reason to be concerned about fair citation in such a broad context of the First Law of Thermodynamics? This is my question, and I am open for professional answers (considering Gentle Science and mentoring early career investigators). For some further priming, the following points are added.
5. It remains unclear to me, why our original wording "energy can neither be produced by mitochondria, nor is there any internal process without energy conservation" was changed in the 'Comment' to the suggestion that there are "frequently made statements that mitochondria ‘create’ or ‘produce’ energy". According to my knowledge of the literature, 'mitochondria create energy' is not a frequently made statement. With close to 370000 publications listed in PubMed on the search term 'mitochondr*' (see Publication efficiency), however, I cannot be sure. I doubt it, but this questionable statement on 'creation of energy' is a matter of proof to be made by the 'Comment'-authors. The only rare example I can come up with is the phrase 'using oxygen to create energy' in a journalist's 'educational' www.nature.com website (https://www.nature.com/scitable/topicpage/mitochondria-14053590/). Skip the 'create' with its rather Godly connotation, and the original "energy can neither be produced" phrase is actually relevant (I try to keep religious and pseudoscientific terminology out of my scientific writing).
6. "How Mitochondria Produce Energy" is a marvellous video full of art (https://www.youtube.com/watch?v=39HTpUG1MwQ), and "Mitochondria and energy production" is another enjoyable video (https://www.youtube.com/watch?v=eOB_M7a9iZ0). A sloppy use of the term 'energy production' is very common in the scientific literature, as is the term 'generation of energy' (but luckily not 'creation'!). Some discussions on the use or abuse of these terms make a rather helpless impression (https://www.researchgate.net/post/Isnt_it_wrong_to_say_that_mitochondria_generate_or_produce_energy).
7. Reference to internal energy transformation (First Law of Thermodynamics) versus external energy transfer in open systems (exchange with the environment) provides the necessary conceptual framework for clarification. This was not really understood by at least one of our coauthors, and neither by the involved reviewers and editors of Nature Metabolism.
8. "We hope that this Comment will stimulate further discussion" — is the comment in the Nature Metabolism Comment. My comment: The discussion could have and should have been made openly before the Nature Metabolism Comment publication — but too many scientists just 'create' publications, without taking the time for quality discussions.

Reference: Harper Mary-Ellen, Patti Mary-Elizabeth (2020) Metabolic terminology: what’s in a name? Nat Metab 2:476-7.

SI units

One year ago, on World Metrology Day (2019-May-20) the redefinition of the SI units came into force. Science faced one of the largest overhauls in history of scientific units. How to commemorate this event of groundbreaking innovation better than with the online publication of Mitochondrial physiology and with the launch of an innovative journal — Bioenergetics Communications.

Versions from MitoFit preprint to BEC reprint

»Versions

This BEC article was communicated as a preprint in MitoFit Preprints

» Gnaiger E, Aasander Frostner E, Abdul Karim N, Abumrad NA, Acuna-Castroviejo D, Adiele RC, et al (2019) Mitochondrial respiratory states and rates. MitoFit Preprint Arch doi:10.26124/mitofit:190001.v4. - »Bioblast link«

Post-publication peer review

This BEC Consortium communication has been rigorously reviewed from pre-print to re-print. Contribute to the discussion to improve the next version of this Living Communication, and upgrade from a reviewer to a coauthor.

» Discussion BEC2020.1

• Please send your comments, full institutional address and preferentially your ORCID to the corresponding author.

MitoPedia topics: BEC 

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Gnaiger E (2021) Bioenergetic cluster analysis – mitochondrial respiratory control in human fibroblasts. MitoFit Preprints 2021.8. https://doi.org/10.26124/mitofit:2021-0008

• Cardoso et al (2021) Magnesium Green for fluorometric measurement of ATP production does not interfere with mitochondrial respiration. Bioenerg Commun 2021.1. doi:10.26124/bec:2021-0001
• Krako Jakovljevic N, Ebanks B, Katyal G, Chakrabarti L, Markovic I, Moisoi N (2021) Mitochondrial homeostasis in cellular models of Parkinson’s Disease. Bioenerg Commun 2021.2. https://doi.org/10.26124/bec:2021-0002
• Went N, Di Marcello M, Gnaiger E (2021) Oxygen dependence of photosynthesis and light-enhanced dark respiration studied by High-Resolution PhotoRespirometry. MitoFit Prep 2021.5. - »Bioblast link«

Gnaiger E (2020) Mitochondrial pathways and respiratory control. An introduction to OXPHOS analysis. 5^th ed. Bioenerg Commun 2020.2. https://doi.org/10.26124/bec:2020-0002

Gnaiger E (2020) Canonical reviewer's comments on: Bureau International des Poids et Mesures (2019) The International System of Units (SI) 9th ed. MitoFit Preprint Arch 2020.4 doi:10.26124/mitofit:200004.

Preprint cited by

Gnaiger E (2019) Editorial: A vision on preprints for mitochondrial physiology and bioenergetics. MitoFit Preprint Arch doi:10.26124/mitofit:190002.v2.

Labels: MiParea: MiP area::Respiration, MiP area::mt-Awareness 

Preparation: Preparation::Permeabilized cells, Preparation::Permeabilized tissue, Preparation::Homogenate, Preparation::Isolated mitochondria  Enzyme: Enzyme::Marker enzyme  Regulation: Topic::Coupling efficiency;uncoupling, Topic::Flux control, Topic::mt-Membrane potential, Topic::Uncoupler  Coupling state: Coupling states::LEAK, Coupling states::OXPHOS, Coupling states::ET  Pathway: Pathways::F, Pathways::N, Pathways::S, Pathways::Gp, Pathways::DQ, Pathways::CIV, Pathways::NS, Pathways::Other combinations, Pathways::ROX  HRR: Instrument and method::O2k-Protocol 

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