Evolutionary bioenergetics of ciliates

Abstract

Understanding why various organisms evolve alternative ways of living requires information on both the fitness advantages of phenotypic modifications and the costs of constructing and operating cellular features. Although the former has been the subject of a myriad of ecological studies, almost no attention has been given to how organisms allocate resources to alternative structures and functions. We address these matters by capitalizing on an array of observations on diverse ciliate species and from the emerging field of evolutionary bioenergetics. A relatively robust and general estimator for the total cost of a cell per cell cycle (in units of ATP equivalents) is provided, and this is then used to understand how the magnitudes of various investments scale with cell size. Among other things, we examine the costs associated with the large macronuclear genomes of ciliates, as well as ribosomes, various internal membranes, osmoregulation, cilia, and swimming activities. Although a number of uncertainties remain, the general approach taken may serve as blueprint for expanding this line of work to additional traits and phylogenetic lineages.

Keywords: Paramecium; Tetrahymena; bioenergetics; ciliates; evolutionary cell biology; osmoregulation; ribosomes; swimming motility.

FIGURE 1

Scaling relationships for maximum growth rates, $R_{\text{max}}$ (defined as the inverse of the cell doubling time, in days) and metabolic rates (molecules of ${\mathrm{O}}_2$/cell/day) as a function of cell dry weight $(B)$ for wide range of ciliate species. The rate of cell division scales negatively with cell dry weight, $R\approx 5.6B^{-0.22},N=89,r^2=0.40,p<{10}^{-10}$, SE of exponent $=0.03$; the metabolic rate scales positively, $M\approx \left(3.4\times {10}^{13}\right)B^{0.62},N=36,r^2=0.72,p<{10}^{-10}$, SE of exponent $=0.07$ Data are contained in Tables S1 and S2

FIGURE 2

(A) Scaling relationship for average swimming speeds $(\nu$, in $\mathrm{\mu }\mathrm{m}/\mathrm{s})$ as a function of cell volume $\left(\mathrm{V}\right.$, in $\mathrm{\mu }{\mathrm{m}}^3$) for 29 ciliate species. The fitted power–law function is $=13{\mathrm{V}}^{0.30},r^2=0.18,p=0.022$, SE of exponent $=0.12$. Data are in Table S3. (B) Scaling relationship for the energetic cost of constructing the ciliar system as a function of cell volume $\left(\mathrm{V}\right.$, in $\mathrm{\mu }{\mathrm{m}}^3$) for 42 ciliate species. The fitted power–law function is $4.9{\mathrm{V}}^{0.83},r^2=0.63,p<{10}^{-9}$, SE of exponent $=0.10$. Data are in Table S4. (C) Scaling relationships for the energetic costs of constructing individual cilia and cirri from a phylogenetic survey. The cost of individual cilia in holotrichs is independent of cell volume, with mean and SE of $22(2)\times {10}^9$ ATP equivalents per cilium. The cost of an average cirrus (in units of ${10}^9\mathrm{A}\mathrm{T}\mathrm{P}$) in hypotrichs scales as $9.6{\mathrm{V}}^{0.39},r^2=0.31.p=0.031$, SE of exponent $=0.16$. Data are in Table S4

FIGURE 3

Scaling relationships for nuclear volumes and surface areas as a function of cell volume for wide range of ciliate species. The power–law relationships scaled against cell volume are $\mathrm{M}\mathrm{V}=2.82{\mathrm{V}}^{0.59},N=51,r^2=0.54,p<{10}^{-9}$, SE of exponent $=0.08$; and $\mathrm{m}\mathrm{V}=0.16{\mathrm{V}}^{0.46},N=31,r^2=0.31,p=0.006$, SE of exponent $=0.12$. All volumes are in units of $\mu {\mathrm{m}}^3.\mathrm{V}$ denotes cell volume, MV macronuclear volume, mV micronuclear volume, and both of the latter are summed over all nuclei when cells contain more than one of either type. For the surface areas of nuclei (in units of ${\mathrm{\mu }\mathrm{m}}^2):\mathrm{M}\mathrm{S}\mathrm{A}=2.34{\mathrm{V}}^{0.54},N=44,r^2=0.53,p<{10}^{-8}$, SE of exponent $=0.08$; and $\mathrm{m}\mathrm{S}\mathrm{A}=0.53{\mathrm{V}}^{0.41},N=28,r^2=0.37,p=0.0004$, SE of exponent $=0.10$