Figures and data in Membranes, energetics, and evolution across the prokaryote-eukaryote divide

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3 figures and 5 tables

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Figure 1

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Scaling features of membrane properties with cell size.

(a) Relationship between the total outer surface area of mitochondria and that of the plasma membrane for all species with available data. Diagonal lines denote three idealized ratios of the two. (b) The number of ATP synthase complexes per cell scales with cell surface area (S, in μm²) as $113 S^{1.26}$ ( $r^{2} = 0.99$ ). (c) Relationship between the total (inner + outer) surface area of mitochondria and cell volume for all species with available data. Open points are extrapolations for species with only outer membrane measures, derived by assuming an inner:outer ratio of 4.6, the average of observations in other species. References to individual data points are provided in Appendix 1–tables 1 and 2.

https://doi.org/10.7554/eLife.20437.003

Figure 2

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The number of ribosomes per cell scales with cell volume (V, in μm³) as 7586V^0.82 (r² = 0.92; SEs of the intercept and slope on the log scale are 0.13 and 0.05, respectively).

Color coding as in previous figures. The data presented in this figure can be found in Figure 2—source data 1; see also Appendix 1–table 3.

https://doi.org/10.7554/eLife.20437.005

Figure 2—source data 1 Source data for Figure 2.: https://doi.org/10.7554/eLife.20437.006
Download elife-20437-fig2-data1-v2.xlsx

Appendix 1—figure 1

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Relative contribution of ATP (P) and NADH/NADPH/FADH $_{2}$ (H) to the biosynthetic costs of lipids and amino acids.

(A) Nonreduced costs including opportunity cost of precursors; (B) Reduced costs without precursors. Amino acid values are obtained from Akashi and Gojobori (2002), assuming growth on glucose.

https://doi.org/10.7554/eLife.20437.011

Tables

Table 1

Contributions of membranes to total cellular growth costs.

Ot denotes the green alga Ostreococcus tauri, Sc the yeast Saccharomyces cerevisiae, Ds the green alga Dunaliella salina, and Ss the pig (Sus scrofa) pancreas cell; references given in Supplementary material. Cell volumes and total membrane areas are in units of μm³ and μm², respectively, with the latter excluding membranes associated with the plastids in the algal species. The fraction of the total cell growth budget allocated to membranes is obtained by the ratio of Equations (1b) and (4), using the species-specific reduced costs in Table 1 where available, and otherwise applying the averages for eukaryotic species; this total cost is then apportioned into five different fractional contributions in the following lines.

https://doi.org/10.7554/eLife.20437.004

	Ot	Sc	Ds	Ss
Cell volume	1	44	591	1060
Total membranes	15	204	2299	12952
Fraction of absolute cell growth budget	0.324	0.096	0.094	0.302
Plasma membrane	0.556	0.328	0.134	0.044
Mitochondria	0.243	0.359	0.197	0.223
Nucleus	0.113	0.085	0.034	0.008
Endoplasmic reticulum + Golgi	0.034	0.111	0.318	0.706
Vesicles/vacuoles	0.055	0.114	0.316	0.019

Appendix 1—table 1

Features of mitochondrial membranes.

Cell volumes are from Lynch and Marinov (2015), in some cases supplemented with additional references from the literature. $V$ : cell volume (in μm³); $S A_{C}$ : cellular surface area (in μm²); $S A_{M I}$ : inner mitochondrial membrane surface area (in μm²); $S A_{M I + M O}$ : inner+outer mitochondrial membrane surface area (in μm²); $M I / M O$ ratio between inner and outer mitochondrial membrane surface area

https://doi.org/10.7554/eLife.20437.012

Species	$V$	$S A_{C}$	$S A_{M I}$	$S A_{M I + M O}$	$M I / M O$	References
Unicellular eukaryotes
Exophiala dermatitidis	43.80	50.95	73.98			Biswas et al. (2003)
Candida albicans	35.36	96.10	37.37			Tanaka et al. (1985); Klis et al. (2014)
Saccharomyces cerevisiae	69.07	61.42	15.83			Uchida et al. (2011)
Tetrahymena pyriformis	16666.00	3014.05	12987.60	83968.50	5.200	Gleason et al. (1975); Poole (1983)
Trichoderma viride	126.70	122.01	139.40			Rosen et al. (1974)
Mammals
Cat, gracilis muscle					2.323	Schwerzmann et al. (1989)
Hamster, intestinal enterocyte	1890.00	5772.00	2668.00	9351.00	3.256	Buschmann and Manke (1981a, 1981b)
Human HeLa cells	2798.67	1178.00	1424.74
Mouse heart					7.020	Kistler and Weber (1975)
Mouse liver					3.540	Kistler and Weber (1975)
Mouse lymphocyte	50.69	88.27	20.43			Al-Hamdani et al. (1979); Mayhew et al. (1979)
Mouse immunoblast	392.98	282.94	143.52			Al-Hamdani et al. (1979)
Mouse pancreas	1434.00	973.00	779.00			Dean (1973)
Pig pancreas cell	1060.00	581.90	460.50	2698.50	4.860	Bolender (1974)
Rat Leydig cell, testes	1210.00	1517.00	1641.00	4561.00	1.779	Mori and Christensen (1980)
Rat liver cell	5100.00	1680.00	7651.65	42615.56	4.718	Weibel et al. (1969); Jakovcic et al. (1978)
Rat heart					12.760	Reith et al. (1973)
Rat L-8 skeletal muscle cell					4.670	Reith et al. (1973)
Land plants and algae
Arabidopsis thaliana, cotyledon	5237.75		1307.00
Chlamydomonas reinhardtii	128.38	129.60	66.82			Calvayrac et al. (1974); Hayashi and Ueda (1989)
Chlorella fusca	102.00	111.40	48.40			Atkinson et al. (1974); Forde et al. (1976)
Dunaliella salina	590.80	322.50	87.40			Maeda and Thompson (1986)
Medicago sativa, meristem	166.90	221.50	16.00			Zhu et al. (1991)
Ochromonas danica					2.450	Smith-Johannsen and Gibbs, 1972
Ostreococcus tauri	0.91	8.30	0.70			Henderson et al. (2007)
Polytoma papillatum	862.54	471.43	778.64			Gaffal et al. (1982)
Rhus toxicodendron	1222.00			1288.50	2.545	Vassilyev (2000)

Appendix 1—table 2

Estimated abundance of ATP synthase complexes in species with quantitative proteomics data.

ATP synthase surface area assumed to be maximum associated with the inner ring, 6.4 × 10⁻⁵m² for bacteria, 1.1 × 10⁻⁴ for eukaryotes. $V$ : cell volume (in μm³); $S A_{C}$ : cellular surface area (in μm²); $N_{P C, r a w}$ : raw protein complex copy number estimates; $N_{P C, c o r r}$ : corrected protein complex copy number estimates; $c_{R}$ : correction factor; $P D$ : packing density (copies/μm²); $f_{S A}$ : fraction of $S A$ : cell division time (hours); $C_{G}$ , $C_{M}$ , $C_{T}$ : costs of building a cell per in 10⁹ ATP equivalents; $C_{G}$ : growth; $C_{M}$ : maintenance (per hours); $C_{T}$ : total; $R_{m a x}$ and $R_{r e d}$ : maximum (all ATP equivalents) and reduced (without ATP equivalents expended in the form of NADH/NADPH/FADH₂) required rate of ATP synthesis (per complex per second) to satisfy lifetime energy requirements.

https://doi.org/10.7554/eLife.20437.013

			F₀F ₁ copies per cell
Species	$V$	$S A_{C}$	$N_{P C, r a w}$	$N_{P C, c o r r}$	$c_{R}$	$P D$	$f_{S A}$	$t$	$C_{G}$	$C_{M}$	$C_{T}$	$R_{m a x}$	$R_{r e d}$	References
Prokaryotes
Bacillus subtilis	1.407	10.69	2435	1602	0.66	150	0.010	1.16	92.51	1.16	93.85	14062	2109	Jeong et al. (1990); Weart et al. (2007); Sharpe et al. (1998)
Escherichia coli	0.983	10.85	1056	3018	2.86	278	0.018	0.99	15.65	0.21	15.86	1475	221	Young (2006); Milo and Phillips, 2016
Leptospira interrogans	0.220	5.72	1187	1344	NA	235	0.015							Beck et al. (2009)
Mycoplasma pneumoniae	0.033	1.32	117	131	1.12	99	0.006	63.74	0.92	0.05	3.87	129	19	Zucker-Franklin et al. (1996a), 1996b
Staphylococcus aureus	0.288	4.00	447	NA	NA	112	0.007							Kehle and Herzog (1989)
Fungi
Saccharomyces cerevisiae (hap)	37.940	64.42	15659	29126	1.86	452	0.050	2.50	2468.20	18.79	2515.15	9598	1440
Schizosaccharomyces pombe	118.000	116.38	65363	70129	1.07	603	0.066	4.31	2347.80	8.70	2385.29	2193	329
Mammals
Homo sapiens , HeLa cell	2798.668	1178.00	1284376	737270	0.57	626	0.068							Borle (1969a, 1969b)
Mus musculus , fibroblast NIH3T3	1765.000	2100.00	1255254	NA	NA	598	0.066							Schwanhäusser et al. (2011)

Appendix 1—table 3

Estimated numbers of ribosomes per cell.

Direct estimates taken from microscopic examinations; proteomic estimates are from averaging of cell-specific estimates for each ribosomal protein subunit. $V$ : cell volume (in μm³); $N_{R, d i r e c t}$ : directly estimated copies per cell; $N_{R, r a w}$ : estimated copies per cell based on proteomics studies. See Figure 2—source data 1 for further details.

https://doi.org/10.7554/eLife.20437.014

Species		$V$	$N_{R, d i r e c t}$	$N_{R, r a w}$	References
Bacteria
Bacillus subtilis		1.44	6000		Barrera and Pan (2004)
				9124	Maass et al. (2011)
Escherichia coli		0.93	72,000		Bremer and Dennis (1996)
			45,100		Fegatella et al. (1998)
			26,300		Fegatella et al. (1998)
			13,500		Fegatella et al. (1998)
			6800		Fegatella et al. (1998)
			55,000		Bakshi et al. (2012)
			20,100
			12,000		Arfvidsson and Wahlund (2003)
				6514	Wiśniewski et al. (2014)
				17,979	Lu et al. (2007)
Legionella pneumophila		0.58	7400		Leskelä et al. (2005)
Leptospira interrogans		0.22	4500		Beck et al. (2009)
				3745	Schmidt et al. (2011)
Mycoplasma pneumonii		0.05	140		Yus et al. (2009)
			300		Seybert et al. (2006)
			140		Kühner et al. (2009)
				255	Maier et al. (2011)
Mycobacterium tuberculosis		0.21	1672		Yamada et al. (2015)
Rickettsia prowazekii		0.09	1500		Pang and Winkler (1994)
Sphingopyxis alaskensis		0.07	1850		Fegatella et al. (1998)
			200		Fegatella et al. (1998)
Spiroplasma melliferum		0.02	275		Ortiz et al. (2006)
Staphylococcus aureus		0.31	54,400		Martin and Iandolo (1975)
Vibrio angustum			27,500		Flärdh et al. (1992)
			8000		Flärdh et al. (1992)
Archaea
ARMAN	undescribed	0.03	92		Comolli et al. (2009)
Eukaryotes
Exophiala dermatitidis		44	195,000		Biswas et al. (2003)
Saccharomyces cerevisiae	haploid	68	200,000		Warner (1999)
			220,000		Yamaguchi et al. (2011)
				134,438	Kulak et al. (2014)
				74,800	Ghaemmaghami et al. (2003)
Schizosaccharomyces pombe		133	150,000		Marguerat et al. (2012)
			500,000		Maclean (1965)
				356,180	Kulak et al. (2014)
				101,099	Marguerat et al. (2012)
Tetrahymena pyriformis		14588	88,900,000		Hallberg and Bruns (1976)
Tetrahymena thermophila		12742	74,000,000		Calzone et al. (1983)
Chlamydomonas reinhardtii	cytoplasm	139	120,500		Bourque et al. (1971)
	chloroplast		55,000
Ostreococcus tauri		0.91	1250		Henderson et al. (2007)
Adonis aestivalis	vegetative	2380	47,700,000		Lin and Gifford (1976)
	transitional	2287	39,066,666
	floral	2690	23,933,333
Glycine max SB-1 cell			9,373,333		Jackson and Lark (1982)
Rhus toxicodendron		1222	2,400,000		Vassilyev (2000)
Zea mays root cell		240,000	25,500,000		Hsiao and (1970)
Hamster, intestinal enterocyte		1890	1,500,000		Buschmann and Manke (1981a, 1981b)
HeLa cell		2800	3,150,000		Duncan and Hershey (1983)
					Zhao et al. (2008)
				4,631,143	Kulak et al. (2014)
Mouse pancreas		1434	1,340,000		Dean (1973)
Rat liver cell		4940	12,700,000		Weibel et al. (1969)

Appendix 1—table 4

Costs of lipids.

The average cost per molecule is calculated for a variety of species using estimates of lipid compositions from the literature and the formulas described in the text. The fraction of fatty acids of given length and saturation level is not shown. Cardiolipin costs are assumed to be 637 (evolutionary) and 236 (reduced) ATP. The cost for molecules in the ‘other’ category is assumed to be the average of glycerophospholipids (GPL) in the species and cardiolipin.

https://doi.org/10.7554/eLife.20437.015

		GPL cost		Composition			Mean cost
Species	Membrane	Tot.	Red.	GPL	Cardiolipin	Other	Tot.	Red.		References
Escherichia coli	Whole cell	367	115	0.926	0.060	0.015	385	124		Haest et al. (1969); Rietveld et al. (1993); Raetz et al. (1979)
Bacillus subtilis	Whole cell	308	102	0.818	0.183	0.000	368	127		Bishop et al. (1967); López et al. (1998)
Caulobacter crescentus	Whole cell	340	111	0.776	0.105	0.119	389	132		Contreras et al. (1978); Chow and Schmidt (1974)
Staphylococcus aureus	Whole cell	323	105	0.931	0.070	0.000	345	114		Haest et al. (1972); Mishra and Bayer (2013)
Zymomonas mobilis	Whole cell	370	118	0.990	0.010	0.000	373	119		Carey and Ingram (1983)
							372	123	mean
							8	3	SE
Candida albicans	Whole cell	338	123	0.934	0.066	0.000	358	131		Goyal and Khuller (1992); Singh et al. (2010)
Chlamydomonas reinhardtii	Whole cell	390	140	0.935	0.065	0.000	406	146		Janero and Barrnett (1981); Giroud et al. (1988); Tatsuzawa et al. (1996)
Debaryomyces hansenii	Whole cell	408	141	0.913	0.087	0.000	428	150		Kaneko et al. (1976)
Dictyostelium discoideum	Whole cell	400	141	0.965	0.014	0.000	395	139		Davidoff and Korn (1963); Ellingson (1974); Weeks and Herring (1980); Paquet et al. (2013)
Paramecium tetraurelia	Whole cell	415	146	0.996	0.004	0.000	415	146
Pichia pastoris	Whole cell	412	144	0.975	0.025	0.000	418	147		Klug et al. (2014)
Saccharomyces cerevisiae	Whole cell	372	133	0.953	0.047	0.000	385	138		Longley et al. (1968); Kaneko et al. (1976); Sharma (2006); Klis et al. (2014)
Schizosaccharomyces pombe	Whole cell	411	142	0.945	0.055	0.000	424	147		Koukou et al. (1990)
							403	143	mean
							8	2	SE
Debaryomyces hansenii	Plasma membrane	398	137	0.913	0.087	0.000	418	146		Kaneko et al. (1976); Turk et al. (2007)
Dictyostelium discoideum	Plasma membrane	414	145	0.980	0.020	0.000	418	147		Weeks and Herring (1980)
Dunaliella salina	Plasma membrane	378	137	1.000	0.000	0.000	378	137		Peeler et al. (1989); Azachi et al. (2002)
Mus musculus , thymocytes	Plasma membrane	409	142	0.921	0.000	0.079	418	145		Van Blitterswijk et al. (1982)
Saccharomyces cerevisiae	Plasma membrane	358	129	0.949	0.035	0.026	375	135		Longley et al. (1968); Zinser et al. (1991); Swan and Watson (1997); Tuller et al. (1999); Blagović et al. (2005)
Schizosaccharomyces pombe	Plasma membrane	411	142	0.856	0.052	0.092	433	151		Koukou et al. (1990)
Vigna radiata , seedling	Plasma membrane	402	141	1.000	0.000	0.000	402	141		Yoshida and Uemura (1986)
							406	143	mean
							8	2	SE
Candida albicans	Mitochondrion	344	125	0.710	0.164	0.126	411	150		Goyal and Khuller (1992)
Danio rerio , whole fish	Mitochondrion	472	162	0.854	0.104	0.042	492	172		Almaida-Pagán et al. (2014)
Pichia pastoris	Mitochondrion	421	145	0.944	0.054	0.002	433	150		Wriessnegger et al. (2009); Klug et al. (2014)
Rattus norwegicus , liver	Mitochondrion	445	154	0.838	0.148	0.024	480	169		Tahin et al. (1981); Colbeau et al. (1971)
Saccharomyces cerevisiae	Mitochondrion	312	116	0.897	0.097	0.006	345	128		Tuller et al. (1999); Zinser et al. (1991); Blagović et al. (2005)
Serripes groenlandicus , gill	Mitochondrion	428	147	0.972	0.028	0.000	434	150		Gillis and Ballantyne (1999)
Sus scrofa , heart	Mitochondrion	409	143	0.797	0.186	0.017	453	161		Comte et al. (1976)
Tetrahymena pyriformis	Mitochondrion	402	144	0.812	0.131	0.057	439	159		Gleason (1976); Nozawa (2011)
							436	155	mean
							16	5	SE

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Michael Lynch
Georgi K Marinov

(2017)

Membranes, energetics, and evolution across the prokaryote-eukaryote divide

eLife 6:e20437.

https://doi.org/10.7554/eLife.20437

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Scaling features of membrane properties with cell size.

The number of ribosomes per cell scales with cell volume (V, in μm3) as 7586V0.82 (r2 = 0.92; SEs of the intercept and slope on the log scale are 0.13 and 0.05, respectively).

Figure 2—source data 1

Relative contribution of ATP (P) and NADH/NADPH/FADH2 (H) to the biosynthetic costs of lipids and amino acids.

Contributions of membranes to total cellular growth costs.

Features of mitochondrial membranes.

Estimated abundance of ATP synthase complexes in species with quantitative proteomics data.

Estimated numbers of ribosomes per cell.

Costs of lipids.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

The number of ribosomes per cell scales with cell volume (V, in μm³) as 7586V^0.82 (r² = 0.92; SEs of the intercept and slope on the log scale are 0.13 and 0.05, respectively).

Relative contribution of ATP (P) and NADH/NADPH/FADH $_{2}$ (H) to the biosynthetic costs of lipids and amino acids.