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

  1. Michael Lynch  Is a corresponding author
  2. Georgi K Marinov
  1. Indiana University, United States
3 figures and 5 tables


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 113S1.26 (r2=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.
The number of ribosomes per cell scales with cell volume (V, in μm3) as 8551V0.79 (r2=0.91; SEs of the intercept and slope on the log scale are 0.14 and 0.06, respectively).

Color coding as in previous figures. References to individual data points are provided in Appendix 1–table 3.
Appendix 1—figure 1
Relative contribution of ATP (P) and NADH/NADPH/FADH2 (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.


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.
Cell volume1445911060
Total membranes15204229912952
Fraction of absolute cell growth budget0.3240.0960.0940.302
Plasma membrane0.5560.3280.1340.044
Endoplasmic reticulum + Golgi0.0340.1110.3180.706
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); SAC: cellular surface area (in μm2); SAMI: inner mitochondrial membrane surface area (in μm2); SAMI+MO: inner+outer mitochondrial membrane surface area (in μm2); MI/MO ratio between inner and outer mitochondrial membrane surface area
Unicellular eukaryotes
Exophiala dermatitidis43.8050.9573.98Biswas et al. (2003)
Candida albicans35.3696.1037.37Tanaka et al. (1985); Klis et al. (2014)
Saccharomyces cerevisiae69.0761.4215.83Uchida et al. (2011)
Tetrahymena pyriformis16666.003014.0512987.6083968.505.200Gleason et al. (1975); Poole (1983)
Trichoderma viride126.70122.01139.40Rosen et al. (1974)
Cat, gracilis muscle2.323Schwerzmann et al. (1989)
Hamster, intestinal enterocyte1890.005772.002668.009351.003.256Buschmann and Manke (1981a, 1981b)
Human HeLa cells2798.671178.001424.74
Mouse heart7.020Kistler and Weber (1975)
Mouse liver3.540Kistler and Weber (1975)
Mouse lymphocyte50.6988.2720.43Al-Hamdani et al. (1979); Mayhew et al. (1979)
Mouse immunoblast392.98282.94143.52Al-Hamdani et al. (1979)
Mouse pancreas1434.00973.00779.00Dean (1973)
Pig pancreas cell1060.00581.90460.502698.504.860Bolender (1974)
Rat Leydig cell, testes1210.001517.001641.004561.001.779Mori and Christensen (1980)
Rat liver cell5100.001680.007651.6542615.564.718Weibel et al. (1969); Jakovcic et al. (1978)
Rat heart12.760Reith et al. (1973)
Rat L-8 skeletal muscle cell4.670Reith et al. (1973)
Land plants and algae
Arabidopsis thaliana, cotyledon5237.751307.00
Chlamydomonas reinhardtii128.38129.6066.82Calvayrac et al. (1974); Hayashi and Ueda (1989)
Chlorella fusca102.00111.4048.40Atkinson et al. (1974); Forde et al. (1976)
Dunaliella salina590.80322.5087.40Maeda and Thompson (1986)
Medicago sativa, meristem166.90221.5016.00Zhu et al. (1991)
Ochromonas danica2.450Smith-Johannsen and Gibbs, 1972
Ostreococcus tauri0.918.300.70Henderson et al. (2007)
Polytoma papillatum862.54471.43778.64Gaffal et al. (1982)
Rhus toxicodendron1222.001288.502.545Vassilyev (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 × 10−5 m2 for bacteria, 1.1 × 10−4 for eukaryotes. V: cell volume (in μm3); SAC: cellular surface area (in μm2); NPC,raw: raw protein complex copy number estimates; NPC,corr: corrected protein complex copy number estimates; cR: correction factor; PD: packing density (copies/μm2); fSA: fraction of SA: cell division time (hours); CG, CM, CT: costs of building a cell per in 109 ATP equivalents; CG: growth; CM: maintenance (per hours); CT: total; Rmax and Rred: 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.
F0F 1 copies per cell
Bacillus subtilis1.40710.69243516020.661500.0101.1692.511.1693.85140622109Jeong et al. (1990); Weart et al. (2007); Sharpe et al. (1998)
Escherichia coli0.98310.85105630182.862780.0180.9915.650.2115.861475221Young (2006); Milo and Phillips, 2016
Leptospira interrogans0.2205.7211871344NA2350.015Beck et al. (2009)
Mycoplasma pneumoniae0.0331.321171311.12990.00663.740.920.053.8712919Zucker-Franklin et al. (1996a), 1996b
Staphylococcus aureus0.2884.00447NANA1120.007Kehle and Herzog (1989)
Saccharomyces cerevisiae (hap)37.94064.4215659291261.864520.0502.502468.2018.792515.1595981440
Schizosaccharomyces pombe118.000116.3865363701291.076030.0664.312347.808.702385.292193329
Homo sapiens , HeLa cell2798.6681178.0012843767372700.576260.068Borle (1969a, 1969b)
Mus musculus , fibroblast NIH3T31765.0002100.001255254NANA5980.066Schwanhäusser 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); NR,direct: directly estimated copies per cell; NR,raw: estimated copies per cell based on proteomics studies
Bacillus subtilis1.4076000Barrera and Pan (2004)
9124Maass et al. (2011)
Escherichia coli0.98372,000Bremer and Dennis (1996)
45,100Fegatella et al. (1998)
26,300Fegatella et al. (1998)
13,500Fegatella et al. (1998)
6800Fegatella et al. (1998)
55,000Bakshi et al. (2012)
12,000Arfvidsson and Wahlund (2003)
6514Wiśniewski et al. (2014)
17,979Lu et al. (2007)
Legionella pneumophila0.5807400Leskelä et al. (2005)
Leptospira interrogans0.2204500Beck et al. (2009)
1039Schmidt et al. (2011)
Mycoplasma pneumonii0.050140Yus et al. (2009)
300Seybert et al. (2006)
422Kühner et al. (2009)
255Maier et al. (2011)
Mycobacterium tuberculosis0.2151672Yamada et al. (2015)
Rickettsia prowazekii0.0891500Pang and Winkler (1994)
Sphingopyxis alaskensis0.0501850Fegatella et al. (1998)
200Fegatella et al. (1998)
Spiroplasma melliferum0.018275Ortiz et al. (2006)
Staphylococcus aureus0.28854,400Martin and Iandolo (1975)
Vibrio angustum27,500Flärdh et al. (1992)
8000Flärdh et al. (1992)
ARMANundescribed0.03092Comolli et al. (2009)
Exophiala dermatitidis43.800195,000Biswas et al. (2003)
Saccharomyces cerevisiaehaploid69.071200,000Warner (1999)
220,000Yamaguchi et al. (2011)
153,456Kulak et al. (2014)
72,284Ghaemmaghami et al. (2003)
Schizosaccharomyces pombe118.000150,000Marguerat et al. (2012)
500,000Maclean (1965)
505,260Kulak et al. (2014)
100,568Marguerat et al. (2012)
Tetrahymena pyriformis14002.0677,490,000Hallberg and Bruns (1976)
Tetrahymena thermophila7856.0074,000,000Calzone et al. (1983)
Chlamydomonas reinhardtiicytoplasm151.000120,500Bourque et al. (1971)
Ostreococcus tauri0.9101250Henderson et al. (2007)
Adonis aestivalisvegetative2380.30047,700,000Lin and Gifford (1976)
Glycine max SB-1 cell9,373,333Jackson and Lark (1982)
Rhus toxicodendron12222,400,000Vassilyev (2000)
Zea mays root cell240,00025,500,000Hsiao and (1970)
Hamster, intestinal enterocyte18901,500,000Buschmann and Manke (1981a, 1981b)
HeLa cell2798.6683,300,000Duncan and Hershey (1983)
Zhao et al. (2008)
5,748,830Kulak et al. (2014)
Mouse pancreas1434.0001,340,000Dean (1973)
Rat liver cell4940.00012,700,000Weibel 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.
GPL costCompositionMean cost
Escherichia coliWhole cell3671150.9260.0600.015385124Haest et al. (1969); Rietveld et al. (1993); Raetz et al. (1979)
Bacillus subtilisWhole cell3081020.8180.1830.000368127Bishop et al. (1967); López et al. (1998)
Caulobacter crescentusWhole cell3401110.7760.1050.119389132Contreras et al. (1978); Chow and Schmidt (1974)
Staphylococcus aureusWhole cell3231050.9310.0700.000345114Haest et al. (1972); Mishra and Bayer (2013)
Zymomonas mobilisWhole cell3701180.9900.0100.000373119Carey and Ingram (1983)
Candida albicansWhole cell3381230.9340.0660.000358131Goyal and Khuller (1992); Singh et al. (2010)
Chlamydomonas reinhardtiiWhole cell3901400.9350.0650.000406146Janero and Barrnett (1981); Giroud et al. (1988); Tatsuzawa et al. (1996)
Debaryomyces hanseniiWhole cell4081410.9130.0870.000428150Kaneko et al. (1976)
Dictyostelium discoideumWhole cell4001410.9650.0140.000395139Davidoff and Korn (1963); Ellingson (1974); Weeks and Herring (1980); Paquet et al. (2013)
Paramecium tetraureliaWhole cell4151460.9960.0040.000415146
Pichia pastorisWhole cell4121440.9750.0250.000418147Klug et al. (2014)
Saccharomyces cerevisiaeWhole cell3721330.9530.0470.000385138Longley et al. (1968); Kaneko et al. (1976); Sharma (2006); Klis et al. (2014)
Schizosaccharomyces pombeWhole cell4111420.9450.0550.000424147Koukou et al. (1990)
Debaryomyces hanseniiPlasma membrane3981370.9130.0870.000418146Kaneko et al. (1976); Turk et al. (2007)
Dictyostelium discoideumPlasma membrane4141450.9800.0200.000418147Weeks and Herring (1980)
Dunaliella salinaPlasma membrane3781371.0000.0000.000378137Peeler et al. (1989); Azachi et al. (2002)
Mus musculus , thymocytesPlasma membrane4091420.9210.0000.079418145Van Blitterswijk et al. (1982)
Saccharomyces cerevisiaePlasma membrane3581290.9490.0350.026375135Longley et al. (1968); Zinser et al. (1991); Swan and Watson (1997); Tuller et al. (1999); Blagović et al. (2005)
Schizosaccharomyces pombePlasma membrane4111420.8560.0520.092433151Koukou et al. (1990)
Vigna radiata , seedlingPlasma membrane4021411.0000.0000.000402141Yoshida and Uemura (1986)
Candida albicansMitochondrion3441250.7100.1640.126411150Goyal and Khuller (1992)
Danio rerio , whole fishMitochondrion4721620.8540.1040.042492172Almaida-Pagán et al. (2014)
Pichia pastorisMitochondrion4211450.9440.0540.002433150Wriessnegger et al. (2009); Klug et al. (2014)
Rattus norwegicus , liverMitochondrion4451540.8380.1480.024480169Tahin et al. (1981); Colbeau et al. (1971)
Saccharomyces cerevisiaeMitochondrion3121160.8970.0970.006345128Tuller et al. (1999); Zinser et al. (1991); Blagović et al. (2005)
Serripes groenlandicus , gillMitochondrion4281470.9720.0280.000434150Gillis and Ballantyne (1999)
Sus scrofa , heartMitochondrion4091430.7970.1860.017453161Comte et al. (1976)
Tetrahymena pyriformisMitochondrion4021440.8120.1310.057439159Gleason (1976); Nozawa (2011)

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  1. Michael Lynch
  2. Georgi K Marinov
Membranes, energetics, and evolution across the prokaryote-eukaryote divide
eLife 6:e20437.