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Research Article

Generalized size scaling of metabolic rates based on single-cell measurements with freshwater phytoplankton

Silvia Zaoli, Andrea Giometto, Emilio Marañón, Stéphane Escrig, Anders Meibom, Arti Ahluwalia, Roman Stocker, View ORCID ProfileAmos Maritan, and Andrea Rinaldo
  1. aLaboratory of Ecohydrology, Institute of Environmental Engineering, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland;
  2. bDepartment of Physics, Harvard University, Cambridge, MA 02138;
  3. cDepartment of Ecology and Animal Biology, Universidad de Vigo, 36210 Vigo, Spain;
  4. dLaboratory of Biological Geochemistry, Institute of Environmental Engineering, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland;
  5. eCentro di Ricerca “E. Piaggio,” Universitá di Pisa, 56126 Pisa, Italy;
  6. fDepartment of Information Engineering, Universitá di Pisa, 56126 Pisa, Italy;
  7. gThe Environmental Microfluidics Laboratory, Department of Environmental Sciences, Eidgenössische Technische Hochschule Zürich, 8092 Zürich, Switzerland;
  8. hDepartment of Physics and Astronomy, Istituto Nazionale di Fisica Nucleare, 35131 Padova, Italy;
  9. iDipartimento di Ingegneria Civile, Edile e Ambientale, Università di Padova, I-35131 Padova, Italy

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PNAS August 27, 2019 116 (35) 17323-17329; first published August 13, 2019; https://doi.org/10.1073/pnas.1906762116
Silvia Zaoli
aLaboratory of Ecohydrology, Institute of Environmental Engineering, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland;
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Andrea Giometto
bDepartment of Physics, Harvard University, Cambridge, MA 02138;
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Emilio Marañón
cDepartment of Ecology and Animal Biology, Universidad de Vigo, 36210 Vigo, Spain;
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Stéphane Escrig
dLaboratory of Biological Geochemistry, Institute of Environmental Engineering, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland;
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Anders Meibom
dLaboratory of Biological Geochemistry, Institute of Environmental Engineering, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland;
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Arti Ahluwalia
eCentro di Ricerca “E. Piaggio,” Universitá di Pisa, 56126 Pisa, Italy;
fDepartment of Information Engineering, Universitá di Pisa, 56126 Pisa, Italy;
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Roman Stocker
gThe Environmental Microfluidics Laboratory, Department of Environmental Sciences, Eidgenössische Technische Hochschule Zürich, 8092 Zürich, Switzerland;
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Amos Maritan
hDepartment of Physics and Astronomy, Istituto Nazionale di Fisica Nucleare, 35131 Padova, Italy;
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  • ORCID record for Amos Maritan
Andrea Rinaldo
aLaboratory of Ecohydrology, Institute of Environmental Engineering, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland;
iDipartimento di Ingegneria Civile, Edile e Ambientale, Università di Padova, I-35131 Padova, Italy
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  • For correspondence: andrea.rinaldo@epfl.ch
  1. Contributed by Andrea Rinaldo, July 1, 2019 (sent for review April 30, 2019; reviewed by Paul G. Falkowski and Pablo A. Marquet)

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Significance

Empirical laws predicting metabolic rates of a species by its average body mass neglect intraspecies variability arising from the range of physiologically feasible rates and phenotypic heterogeneity. We describe an exploratory experimental test of a theory that explicitly accounts for such variations. We show, by single-cell joint measurements of mass and uptake rates, how marginal distributions of mass and rates collapse onto a common master distribution for species spanning 3 orders of magnitude in cell volume. These results demonstrate the potential of a generalized scaling theory that goes beyond population averages to incorporate within-species variation.

Abstract

Kleiber’s law describes the scaling of metabolic rate with body size across several orders of magnitude in size and across taxa and is widely regarded as a fundamental law in biology. The physiological origins of Kleiber’s law are still debated and generalizations of the law accounting for deviations from the scaling behavior have been proposed. Most theoretical and experimental studies of Kleiber’s law, however, have focused on the relationship between the average body size of a species and its mean metabolic rate, neglecting intraspecific variation of these 2 traits. Here, we propose a theoretical characterization of such variation and report on proof-of-concept experiments with freshwater phytoplankton supporting such framework. We performed joint measurements at the single-cell level of cell volume and nitrogen/carbon uptake rates, as proxies of metabolic rates, of 3 phytoplankton species using nanoscale secondary ion mass spectrometry (NanoSIMS) and stable isotope labeling. Common scaling features of the distribution of nutrient uptake rates and cell volume are found to hold across 3 orders of magnitude in cell size. Once individual measurements of cell volume and nutrient uptake rate within a species are appropriately rescaled by a function of the average cell volume within each species, we find that intraspecific distributions of cell volume and metabolic rates collapse onto a universal curve. Based on the experimental results, this work provides the building blocks for a generalized form of Kleiber’s law incorporating intraspecific, correlated variations of nutrient-uptake rates and body sizes.

  • phenotypic heterogeneity
  • Synechococcus
  • Scenedesmus
  • Cryptomonas
  • metabolic theory of ecology

Footnotes

  • ↵1To whom correspondence may be addressed. Email: andrea.rinaldo{at}epfl.ch.
  • Author contributions: A. Maritan and A.R. designed research; S.Z., A.G., E.M., and A. Meibom performed research; S.Z., E.M., S.E., A. Meibom, and R.S. contributed new reagents/analytic tools; S.Z., A.G., E.M., S.E., A.A., R.S., A. Maritan, and A.R. analyzed data; and S.Z., A.G., E.M., A.A., R.S., A. Maritan, and A.R. wrote the paper.

  • Reviewers: P.G.F., Rutgers University; and P.A.M., Pontificia Universidad del Chile.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1906762116/-/DCSupplemental.

  • Copyright © 2019 the Author(s). Published by PNAS.

This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

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Generalized size scaling of metabolic rates based on single-cell measurements with freshwater phytoplankton
Silvia Zaoli, Andrea Giometto, Emilio Marañón, Stéphane Escrig, Anders Meibom, Arti Ahluwalia, Roman Stocker, Amos Maritan, Andrea Rinaldo
Proceedings of the National Academy of Sciences Aug 2019, 116 (35) 17323-17329; DOI: 10.1073/pnas.1906762116

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Generalized size scaling of metabolic rates based on single-cell measurements with freshwater phytoplankton
Silvia Zaoli, Andrea Giometto, Emilio Marañón, Stéphane Escrig, Anders Meibom, Arti Ahluwalia, Roman Stocker, Amos Maritan, Andrea Rinaldo
Proceedings of the National Academy of Sciences Aug 2019, 116 (35) 17323-17329; DOI: 10.1073/pnas.1906762116
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