The metabolic basis of whole-organism RNA and phosphorus content

doi:10.1073/pnas.0504756102

The metabolic basis of whole-organism RNA and phosphorus content

^*Department of Biology, University of New Mexico, Albuquerque, NM 87131; ^‡National Center for Ecological Analysis and Synthesis, Santa Barbara, CA 93101; ^§Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501; ^∥Department of Zoology and Physiology, University of Wyoming, Laramie, WY 82071; ^¶Department of Biology, Arizona State University, Tempe, AZ 85287-1501; ^**Theoretical Division T8 MS B285 and ^††Bioscience Division B4 MS J585, Los Alamos National Laboratory, Los Alamos, NM 87545; and ^‡‡Section of Integrative Biology, University of Texas, Austin, TX 78712

Communicated by Mimi A. R. Koehl, University of California, Berkeley, CA, June 18, 2005 (received for review April 21, 2004)

Abstract

Understanding the storage, flux, and turnover of nutrients in organisms is important for quantifying contributions of biota to biogeochemical cycles. Here we present a model that predicts the storage of phosphorus-rich RNA and whole-body phosphorus content in eukaryotes based on the mass- and temperature-dependence of ATP production in mitochondria. Data from a broad assortment of eukaryotes support the model's two main predictions. First, whole-body RNA concentration is proportional to mitochondrial density and consequently scales with body mass to the -1/4 power. Second, whole-body phosphorus content declines with increasing body mass in eukaryotic unicells but approaches a relatively constant value in large multicellular animals because the fraction of phosphorus in RNA decreases relative to the fraction in other pools. Extension of the model shows that differences in the flux of RNA-associated phosphorus are due to the size dependencies of metabolic rate and RNA concentration. Thus, the model explicitly links two biological currencies at the individual level: energy in the form of ATP and materials in the form of phosphorus, both of which are critical to the functioning of ecosystems. The model provides a framework for linking attributes of individuals to the storage and flux of phosphorus in ecosystems.

Footnotes

↵ † To whom correspondence should be sent at the present address: Department of Zoology, University of Florida, P.O. Box 118525, Gainesville, FL 32611. E-mail: gillooly{at}unm.edu.
Author contributions: J.F.G. and A.P.A. designed research; J.F.G., A.P.A., J.H.B., J.J.E, C.M.d.R., V.M.S., G.B.W., W.H.W., and H.A.W. performed research; J.F.G., A.P.A., V.M.S., G.B.W., W.H.W., and H.A.W. contributed new reagents/analytic tools; J.F.G. and A.P.A. analyzed data; and J.F.G., A.P.A., J.H.B., J.J.E., C.M.d.R., V.M.S., G.B.W., W.H.W., and H.A.W. wrote the paper.