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Achieving Temperature-Size Changes in a Unicellular Organism

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Achieving Temperature-Size Changes in a Unicellular Organism The ISME Journal (2013) 7, 28–36 & 2013 International Society for Microbial Ecology All rights reserved 1751-7362/13 www.nature.com/ismej ORIGINAL ARTICLE Achieving temperature-size changes in a unicellular organism Jack Forster1, Andrew G Hirst1 and Genoveva F Esteban2 1School of Biological and Chemical Sciences, Queen Mary University of London, London, UK and 2Conservation Ecology and Environmental Sciences Group, School of Applied Sciences, Bournemouth University, Dorset, UK 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 480% 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. The ISME Journal (2013) 7, 28–36; doi:10.1038/ismej.2012.76; published online 26 July 2012 Subject Category: microbial population and community ecology Keywords: Cyclidium glaucoma; development; growth; temperature-size rule Introduction about, and how it impacts on the ecology of ectothermic species. The temperature-size rule (TSR) is a ubiquitous Despite the ubiquity of the TSR, the effect of intraspecific phenomenon affecting most (480%) temperature on organism body size remains poorly ectotherms: individuals reared at cooler tempera- understood. There has recently been a significant tures mature at a larger size than those reared at amount of work on how the TSR is established in warmer temperatures (Atkinson, 1994). The rule is multicellular organisms, with studies investigating common both in multicellular (Atkinson 1994; how and when size changes occur during the life Forster et al., 2011a, b) and in unicellular organisms, cycle (Karan et al., 1998; Petersen et al., 2000; having been found in bacteria and many protists Forster and Hirst, 2011; Potter et al., 2011). Further, (Montagnes and Franklin, 2001; Atkinson et al., differences in the thermal sensitivities of growth 2003). Recently, reduced body sizes at both the and development rates during ontogeny have been species and community level have been identi- shown to drive and maintain the TSR in multi- fied as a universal ecological response to global cellular organisms (Forster et al., 2011a, b). Cur- warming (Daufresne et al., 2009; Gardner et al., rently, such empirical study of how the TSR is 2011; Sheridan and Bickford, 2011). Therefore, established in unicellular organisms does not exist. we need to understand how the TSR is brought A simple conceptual model has demonstrated that the mechanism underpinning the TSR must be Correspondence: AG Hirst, School of Biological and Chemical different in unicellular and multicellular organisms Sciences, Queen Mary University of London, Mile End Road, (Forster et al., 2011a). This difference is highlighted London E1 4NS, UK. by the equation that links size and rates: E-mail: [email protected] g M or GF Esteban, Conservation Ecology and Environmental Sciences ¼ ln A ð1Þ Group, School of Applied Sciences, Bournemouth University, D MP Talbot Campus, Poole, Dorset BH12 5BB, UK. where g is the mass-specific growth rate of the E-mail: [email protected] À 1 Received 9 February 2012; revised 22 May 2012; accepted 1 June individual (day ), D is the development rate À 1 2012; published online 26 July 2012 (day , that is, 1/doubling time), MA is the mass of Unicellular temperature-size changes J Forster et al 29 the adult and MP is the mass of a single progeny. multicellular organisms remains theoretical: we still We use the term ‘adult’ here to refer to the mass of require testing of changes in mother and daughter a mother cell at the point of division in unicells. size during the acclimation phase in unicellular Similarly, ‘progeny’ (referring to eggs in multi- organisms. Studies of unicellular organisms typi- cellular organisms) refers to a single daughter cell cally allow species to acclimate to new temperatures just after division of the mother cell. We use the before carrying out size measurements (for example, exponential form of the model in Equation 1 (Forster five generations; Montagnes and Franklin, 2001). et al., 2011a), as this most accurately represents However, we need to understand when, and for how individual growth of unicells (Krasnow, 1978; Olson long, mother and daughter sizes become decoupled. et al., 1986). In multicellular organisms, changes Such research will show whether fundamental life- in size have been shown to differ in adults and history rates relevant to all living organisms, growth progeny. Size changes in acclimated adults are and development (Equation 1), respond differently B2.5% 1C À 1 but o1% 1C À 1 in progeny. This cannot to temperature in different groups. We carry out this be the case in unicells: dividing in half requires the research here by measuring cell size changes in TSR to equally impact mother and daughter size in the ciliated protozoan Cyclidium glaucoma during unicells at acclimation. This in turn means the rates thermal acclimation. Further, including parameters driving the TSR, growth and development, can only for temperature, time and population abundance become temporarily decoupled during acclimation within a general linear model (GLM), we can in unicells (Figure 1). This temporary decoupling ascertain and account for the impact of population suggests a fundamentally different mechanism of abundance on cell size during the acclimation and the TSR in unicellular compared with multicellular thus singularly determine the importance of tem- organisms, where rates remain decoupled (Forster perature in determining cell size. et al., 2011a), despite both groups obeying the Along with understanding how size changes are TSR. Currently, this disparity between uni- and brought about in unicells at an individual level, we need to understand the potential impact of the TSR on carrying capacity and biomass. There have been Size acclimatedSize acclimation Size acclimated few studies examining the impact of temperature 17°C on these traits in unicellular organisms: previous Temperature ecological theory predicts carrying capacity (defined M change A0 here as the number of organisms supported in a M given volume) to decrease with increasing tempera- P1 25°C 25°C ture, following an Arrhenius function (Savage et al., 2004), thus we may expect maximum number of MA1 individuals in a culture to decrease with increasing temperature. Further, mesocosm experiments inves- MP2 tigating the impact of temperature on freshwater phytoplankton found higher temperatures to be MA2 MA5 = MA6 associated with a reduced total biomass (Yvon- MA0 = MA1 MP5 = MP6 = MP 7 Durocher et al., 2011). However, this was not MP1 = MP2 M P3 conducted at an individual species level, thus we MA3 M /M = ln2 do not know whether changes in biomass are related MAn /MPn = ln2 An Pn g/D = ln2 g /D = ln2 MP4 to shifts towards smaller species or intraspecific size * MA4 changes. Here, we compare carrying capacity and MP5 biomass (the product of carrying capacity and mean ≠ ≠ M MA2 MA3 MA4 A5 cell volume (MCV)) in C. glaucoma across a range of M ≠ M ≠ M P3 P4 Px MP6 temperatures to see whether these traits do indeed M A6 scale negatively with temperature. ≠ M MAn /MPn ln2 P7 Using the ciliate species C. glaucoma, we shall ≠ g/D ln2 therefore address the following questions: How do *completion of mother and daughter cell sizes change when g and D adjustment acclimating to a novel thermal environment? Does carrying capacity scale negatively with temperature Figure 1 A hypothetical example of the effect of temperature in C. glaucoma? Finally, how does temperature change on a unicellular organism which adheres to the TSR, impact on the maximum biomass of C. glaucoma where MA ¼ adult mass (mother cell), MP ¼ progeny mass (daughter cell) and subscript numbers represent generation number. The populations? organism starts at 17 1C, MA/MP is a fixed ratio and thus g/D is fixed too. The organism is then displaced into an environment at 25 1C (indicated by the vertical arrow), as cell size must change, the g/D ratio must become temporarily decoupled. Finally, g/D Materials and methods 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 The protist species C. glaucoma was chosen due to attain an acclimated size (MPn to MAn). its short generation times; having a standard geometric The ISME Journal Unicellular temperature-size changes J Forster et al 30 shape, such that cell volumes could be accurately randomly selected squares, and the mean number of determined from length and width measurements; cells calculated per 1 ml. Thirty individual cells and individuals undergoing fixation in formalin were randomly selected, photographed under a maintaining an excellent cell structure. Ten sterile  100 magnification optical microscope and then culture flasks (30 ml flasks, Corning Incorporated, measurements of length and width (mm) made from Corning, NY, USA) were prepared for C.
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