Diatom growth responses to photoperiod and light are predictable from diel reductant generation

Abstract

Light drives phytoplankton productivity, so phytoplankton must exploit variable intensities and durations of light exposure, depending upon season, latitude, and depth. We analyzed the growth, photophysiology and composition of small, Thalassiosira pseudonana, and large, Thalassiosira punctigera, centric diatoms from temperate, coastal marine habitats, responding to a matrix of photoperiods and growth light intensities. T. pseudonana showed fastest growth rates under long photoperiods and low to moderate light intensities, while the larger T. punctigera showed fastest growth rates under short photoperiods and higher light intensities. Photosystem II function and content responded primarily to instantaneous growth light intensities during the photoperiod, while diel carbon fixation and RUBISCO content responded more to photoperiod duration than to instantaneous light intensity. Changing photoperiods caused species-specific changes in the responses of photochemical yield (e^- /photon) to growth light intensity. These photophysiological variables showed complex responses to photoperiod and to growth light intensity. Growth rate also showed complex responses to photoperiod and growth light intensity. But these complex responses resolved into a close relation between growth rate and the cumulative daily generation of reductant, across the matrix of photoperiods and light intensities.

Keywords: RUBISCO; Thalassiosira; cell size; diatom; electron transport; growth; photoperiod; photosystem II.

Figure 1

Cell specific exponential growth rate (μ, d⁻¹) as a function of culture growth light intensity during the photoperiod (μmol photons · m⁻² · s⁻¹) (A, B) or of daily cumulative photons (μmol photons · m⁻² · d⁻¹) (C, D) for a small diatom Thalassiosira pseudonana (A, C) or a large diatom Thalassiosira punctigera (B, D) at light:dark (L:D) cycles of 24:0 (filled circles), 16:8 (open circles), 8:16 (open triangles), and 4:20 (filled triangles). Points show average growth rate determinations from two or three independently grown cultures; the range of replicated points falls within the symbol size. Solid lines in A and B show light intensity response curves of growth rate fitted with the equation of (Peeters and Eilers 1978, Eilers and Peeters, 1988). Bold line in C shows linear regression of pooled μ to daily cumulative photons under subsaturating growth light conditions; thin dashed lines show 95% confidence intervals on the fitted curves.

Figure 2

Maximum cell specific exponential growth rate (A, μ_max, d⁻¹) and saturation growth light (K_L) (B, μmol photons · m⁻² · s⁻¹) derived from the growth versus irradiance curves (Fig. 1, A and B), plotted as a function of photoperiod for T. pseudonana (open circles) and T. punctigera (filled circles). Solid lines in A show single phase exponential rise to a plateau for T. pseudonana, and a linear decrease for T. punctigera; thin dashed lines show 95% confidence intervals on the fitted curves. Error bars on points show the 95% confidence intervals on the fitted parameters, derived from the curves in Figure 1.

Figure 3

Photosystem II electron transport rate (e⁻ · PSII ⁻¹ · s⁻¹) under illumination (A, B) and PSII _active content (fmol · μg protein⁻¹) (C, D) versus growth light (μmol photons · m⁻² · s⁻¹) for T. pseudonana (A, C) and T. punctigera (B, D) at L:D cycles of 24:0 (filled circles), 16:8 (open circles), 8:16 (open triangles), and 4:20 (filled triangles). Points show averages from each of 2 or 3 independently grown cultures; error bars show range of 2 replicated points and standard deviation of 3 replicated points, often within symbols. Each replicate was in turn each based upon an average of 5–9 repeated determinations taken within a diel cycle from a culture.

Figure 4

Apparent carbon assimilation per RUBISCO active site (C · RbcL⁻¹ · s⁻¹) under illumination (A, B) and RbcL content (fmol · μg protein⁻¹) (C, D) versus growth light (μmol photons · m⁻² · s⁻¹) for T. pseudonana (A, C) and T. punctigera (B, D) at L:D cycles of 24:0 (filled circles), 16:8 (open circles), 8:16 (open triangles), and 4:20 (filled triangles). Points show averages from each of 2 or 3 independently grown cultures; error bars show range of 2 replicated points and standard deviation of 3 replicated points, often within symbols. Each replicate was in turn each based upon an average of 5–9 repeated determinations taken within a diel cycle from a culture.

Figure 5

Carbon fixation rate per cellular total protein (pmol C · μg protein⁻¹ · s⁻¹) as a function of electron transport rate per total protein (pmol e⁻ · μg protein⁻¹ · s⁻¹) for T. pseudonana (A) or T. punctigera (B) under L:D cycles of 24:0 (filled circles), 16:8 (open circles), 8:16 (open triangles), and 4:20 (filled triangles). The fine dotted line shows the theoretical maximum of 1C: 4 e⁻, assuming the 4 e⁻ reduction in CO ₂ to (CH ₂O) and no diversion of electrons to other metabolic pathways. Cell specific exponential growth rate (μ, d⁻¹) as a function of daily cumulative electron transport rate per total protein (μmol e⁻ · μg protein⁻¹ · d⁻¹) for T. pseudonana (C) or T. punctigera (D). Solid lines: fitted curve with the growth‐irradiance equation (A, C) or linear regression (B, D); thin dashed lines show 95% confidence intervals on the fitted curves. Oval in A outlines T. pseudonana measures from 24:0 L:D cycle at 300 μmol photons · m⁻² · d⁻¹ excluded from the curve fit. Measurements from the same samples in the oval in C were included in the curve fit. Ovals in B and D outline T. punctigera under 4:20 L:D cycles, excluded from the linear regression.

Figure 6

Carbon fixation per PSII transported electron (C/e⁻) versus daily cumulative photons (μmol photons · m⁻² · d⁻¹) for (A) T. pseudonana and (B) T. punctigera under L:D cycles of 24:0 (filled circles), 16:8 (open circles), 8:16 (open triangles), and 4:20 (filled triangles). Points show averages from 2 or 3 independently grown cultures; error bars show range of duplicated points and standard deviation of triplicated points, many bars fall within the size of the symbols. Horizontal dotted line shows 0.25 theoretical maximum 1C: 4 e⁻.