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Achieving temperature-size changes in a unicellular organism.

Forster J, Hirst AG, Esteban GF - ISME J (2012)

Bottom Line: Thermal acclimation is rapid, being completed within approximately a single generation.Further, we examine the impact of increased temperatures on carrying capacity and total biomass, to investigate potential adaptive strategies of size change.We demonstrate no temperature effect on carrying capacity, but maximum supported biomass to decrease with increasing temperature.

View Article: PubMed Central - PubMed

Affiliation: School of Biological and Chemical Sciences, Queen Mary University of London, London, UK.

ABSTRACT
The temperature-size rule (TSR) is an intraspecific phenomenon describing the phenotypic plastic response of an organism size to the temperature: individuals reared at cooler temperatures mature to be larger adults than those reared at warmer temperatures. The TSR is ubiquitous, affecting >80% species including uni- and multicellular groups. How the TSR is established has received attention in multicellular organisms, but not in unicells. Further, conceptual models suggest the mechanism of size change to be different in these two groups. Here, we test these theories using the protist Cyclidium glaucoma. We measure cell sizes, along with population growth during temperature acclimation, to determine how and when the temperature-size changes are achieved. We show that mother and daughter sizes become temporarily decoupled from the ratio 2:1 during acclimation, but these return to their coupled state (where daughter cells are half the size of the mother cell) once acclimated. Thermal acclimation is rapid, being completed within approximately a single generation. Further, we examine the impact of increased temperatures on carrying capacity and total biomass, to investigate potential adaptive strategies of size change. We demonstrate no temperature effect on carrying capacity, but maximum supported biomass to decrease with increasing temperature.

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A hypothetical example of the effect of temperature change on a unicellular organism which adheres to the TSR, where MA=adult mass (mother cell), MP=progeny mass (daughter cell) and subscript numbers represent generation number. The organism starts at 17 °C, MA/MP is a fixed ratio and thus g/D is fixed too. The organism is then displaced into an environment at 25 °C (indicated by the vertical arrow), as cell size must change, the g/D ratio must become temporarily decoupled. Finally, g/D returns to a fixed state of ln2 (0.69, in this example at the fourth generation, between MP4 and MA4) and adult and progeny size attain an acclimated size (MPn to MAn).
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fig1: A hypothetical example of the effect of temperature change on a unicellular organism which adheres to the TSR, where MA=adult mass (mother cell), MP=progeny mass (daughter cell) and subscript numbers represent generation number. The organism starts at 17 °C, MA/MP is a fixed ratio and thus g/D is fixed too. The organism is then displaced into an environment at 25 °C (indicated by the vertical arrow), as cell size must change, the g/D ratio must become temporarily decoupled. Finally, g/D returns to a fixed state of ln2 (0.69, in this example at the fourth generation, between MP4 and MA4) and adult and progeny size attain an acclimated size (MPn to MAn).

Mentions: where g is the mass-specific growth rate of the individual (day−1), D is the development rate (day−1, that is, 1/doubling time), MA is the mass of the adult and MP is the mass of a single progeny. We use the term ‘adult' here to refer to the mass of a mother cell at the point of division in unicells. Similarly, ‘progeny' (referring to eggs in multicellular organisms) refers to a single daughter cell just after division of the mother cell. We use the exponential form of the model in Equation 1 (Forster et al., 2011a), as this most accurately represents individual growth of unicells (Krasnow, 1978; Olson et al., 1986). In multicellular organisms, changes in size have been shown to differ in adults and progeny. Size changes in acclimated adults are ∼2.5% °C−1 but <1% °C−1 in progeny. This cannot be the case in unicells: dividing in half requires the TSR to equally impact mother and daughter size in unicells at acclimation. This in turn means the rates driving the TSR, growth and development, can only become temporarily decoupled during acclimation in unicells (Figure 1). This temporary decoupling suggests a fundamentally different mechanism of the TSR in unicellular compared with multicellular organisms, where rates remain decoupled (Forster et al., 2011a), despite both groups obeying the TSR. Currently, this disparity between uni- and multicellular organisms remains theoretical: we still require testing of changes in mother and daughter size during the acclimation phase in unicellular organisms. Studies of unicellular organisms typically allow species to acclimate to new temperatures before carrying out size measurements (for example, five generations; Montagnes and Franklin, 2001). However, we need to understand when, and for how long, mother and daughter sizes become decoupled. Such research will show whether fundamental life-history rates relevant to all living organisms, growth and development (Equation 1), respond differently to temperature in different groups. We carry out this research here by measuring cell size changes in the ciliated protozoan Cyclidium glaucoma during thermal acclimation. Further, including parameters for temperature, time and population abundance within a general linear model (GLM), we can ascertain and account for the impact of population abundance on cell size during the acclimation and thus singularly determine the importance of temperature in determining cell size.


Achieving temperature-size changes in a unicellular organism.

Forster J, Hirst AG, Esteban GF - ISME J (2012)

A hypothetical example of the effect of temperature change on a unicellular organism which adheres to the TSR, where MA=adult mass (mother cell), MP=progeny mass (daughter cell) and subscript numbers represent generation number. The organism starts at 17 °C, MA/MP is a fixed ratio and thus g/D is fixed too. The organism is then displaced into an environment at 25 °C (indicated by the vertical arrow), as cell size must change, the g/D ratio must become temporarily decoupled. Finally, g/D returns to a fixed state of ln2 (0.69, in this example at the fourth generation, between MP4 and MA4) and adult and progeny size attain an acclimated size (MPn to MAn).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3526166&req=5

fig1: A hypothetical example of the effect of temperature change on a unicellular organism which adheres to the TSR, where MA=adult mass (mother cell), MP=progeny mass (daughter cell) and subscript numbers represent generation number. The organism starts at 17 °C, MA/MP is a fixed ratio and thus g/D is fixed too. The organism is then displaced into an environment at 25 °C (indicated by the vertical arrow), as cell size must change, the g/D ratio must become temporarily decoupled. Finally, g/D returns to a fixed state of ln2 (0.69, in this example at the fourth generation, between MP4 and MA4) and adult and progeny size attain an acclimated size (MPn to MAn).
Mentions: where g is the mass-specific growth rate of the individual (day−1), D is the development rate (day−1, that is, 1/doubling time), MA is the mass of the adult and MP is the mass of a single progeny. We use the term ‘adult' here to refer to the mass of a mother cell at the point of division in unicells. Similarly, ‘progeny' (referring to eggs in multicellular organisms) refers to a single daughter cell just after division of the mother cell. We use the exponential form of the model in Equation 1 (Forster et al., 2011a), as this most accurately represents individual growth of unicells (Krasnow, 1978; Olson et al., 1986). In multicellular organisms, changes in size have been shown to differ in adults and progeny. Size changes in acclimated adults are ∼2.5% °C−1 but <1% °C−1 in progeny. This cannot be the case in unicells: dividing in half requires the TSR to equally impact mother and daughter size in unicells at acclimation. This in turn means the rates driving the TSR, growth and development, can only become temporarily decoupled during acclimation in unicells (Figure 1). This temporary decoupling suggests a fundamentally different mechanism of the TSR in unicellular compared with multicellular organisms, where rates remain decoupled (Forster et al., 2011a), despite both groups obeying the TSR. Currently, this disparity between uni- and multicellular organisms remains theoretical: we still require testing of changes in mother and daughter size during the acclimation phase in unicellular organisms. Studies of unicellular organisms typically allow species to acclimate to new temperatures before carrying out size measurements (for example, five generations; Montagnes and Franklin, 2001). However, we need to understand when, and for how long, mother and daughter sizes become decoupled. Such research will show whether fundamental life-history rates relevant to all living organisms, growth and development (Equation 1), respond differently to temperature in different groups. We carry out this research here by measuring cell size changes in the ciliated protozoan Cyclidium glaucoma during thermal acclimation. Further, including parameters for temperature, time and population abundance within a general linear model (GLM), we can ascertain and account for the impact of population abundance on cell size during the acclimation and thus singularly determine the importance of temperature in determining cell size.

Bottom Line: Thermal acclimation is rapid, being completed within approximately a single generation.Further, we examine the impact of increased temperatures on carrying capacity and total biomass, to investigate potential adaptive strategies of size change.We demonstrate no temperature effect on carrying capacity, but maximum supported biomass to decrease with increasing temperature.

View Article: PubMed Central - PubMed

Affiliation: School of Biological and Chemical Sciences, Queen Mary University of London, London, UK.

ABSTRACT
The temperature-size rule (TSR) is an intraspecific phenomenon describing the phenotypic plastic response of an organism size to the temperature: individuals reared at cooler temperatures mature to be larger adults than those reared at warmer temperatures. The TSR is ubiquitous, affecting >80% species including uni- and multicellular groups. How the TSR is established has received attention in multicellular organisms, but not in unicells. Further, conceptual models suggest the mechanism of size change to be different in these two groups. Here, we test these theories using the protist Cyclidium glaucoma. We measure cell sizes, along with population growth during temperature acclimation, to determine how and when the temperature-size changes are achieved. We show that mother and daughter sizes become temporarily decoupled from the ratio 2:1 during acclimation, but these return to their coupled state (where daughter cells are half the size of the mother cell) once acclimated. Thermal acclimation is rapid, being completed within approximately a single generation. Further, we examine the impact of increased temperatures on carrying capacity and total biomass, to investigate potential adaptive strategies of size change. We demonstrate no temperature effect on carrying capacity, but maximum supported biomass to decrease with increasing temperature.

Show MeSH
Related in: MedlinePlus