Photoacclimation of the polar diatom Chaetoceros neogracilis at low temperature

Abstract

Polar microalgae face two major challenges: 1- growing at temperatures (-1.7 to 5°C) that limit enzyme kinetics; and 2- surviving and exploiting a wide range of irradiance. The objective of this study is to understand the adaptation of an Arctic diatom to its environment by studying its ability to acclimate to changes in light and temperature. We acclimated the polar diatom Chaetoceros neogracilis to various light levels at two different temperatures and studied its growth and photosynthetic properties using semi-continuous cultures. Rubisco content was high, to compensate for low catalytic rates, but did not change detectably with growth temperature. Contrary to what is observed in temperate species, in C. neogracilis, carbon fixation rate (20 min 14C incorporation) equaled net growth rate (μ) suggesting very low or very rapid (<20 min) re-oxidation of the newly fixed carbon. The comparison of saturation irradiances for electron transport, oxygen net production and carbon fixation revealed alternative electron pathways that could provide energy and reducing power to the cell without consuming organic carbon which is a very limiting product at low temperatures. High protein contents, low re-oxidation of newly fixed carbon and the use of electron pathways alternative to carbon fixation may be important characteristics allowing efficient growth under those extreme environmental conditions.

Fig 1

(A) Growth rate of C. neogracilis cultures versus growth irradiance at 0°C (circles) and 5°C (triangles). A Poisson function was fitted to the data and gives an estimate of μ_max of 0.63 d^-1 and a K_E of 19 μmol photon m^-2 s^-1 at 0°C and a μ_max of 1.1 d^-1 and a K_E of 35 μmol photon m^-2 s^-1 at 5°C. (B) Chl a: C ratio of C. neogracilis cells versus growth irradiance at 0°C (circles) and 5°C (triangles). In (A) each data point is the mean growth rate of 3 cultures measured each day over 10 consecutive days. In (B), each data point is the mean of 3 cultures measured each day over 3 consecutive days (23, 50, 80, 150, 400 μmol photon m^-2 s^-1) or 2 days (10 μmol photon m^-2 s^-1). Error bars represent standard deviations.

Fig 2. Photoacclimation of carbon fixation.

E_K^C (A), and α* (B) versus growth irradiance at 0°C (circles) and 5°C (triangles). P^C_m (squares), P^C_e (diamonds) and μ (hexagons) versus growth irradiance at 0°C (C) and 5°C (D). P^C_e versus μ (E) and P^C_m versus μ at 0°C (circles) and 5°C (triangle). Each data point is the mean of 3 cultures measured each day during 3 consecutive days (50, 80, 400 μmol photon m^-2 s^-1) or 2 days (10 μmol photon m^-2 s^-1). In A, E, F, the dotted lines represent the 1:1 line Error bars represent standard deviations.

Fig 3. Photoacclimation of the Rubisco content.

Rubisco content versus growth irradiance at 0°C (circles) and 5°C (triangles). The grey line represents the mean rubisco content measured in various mesophilic diatoms (Thalassiosira weissflogii, Thalassiosira oceanica, Skeletonema costatum, Chaetoceros muelleri, Phaeodactylum tricornutum from Losh et al. (2013)). Dashed lines represent standard deviations. Each data point is the mean of 3 cultures measured each day during 3 consecutive days (23, 50, 80, 150, 400 μmol photon m^-2 s^-1) or 2 days (10 μmol photon m^-2 s^-1). Error bars represent standard deviations.

Fig 4. Effect of the acclimation irradiance on the xanthophyll cycle of C. neogracilis.

(Dt +Dd)/Chl a (A) and Dt / Chl a (C) versus growth irradiance at 0°C (circles) and 5°C (triangles). (Dt +Dd) / Chl a (B) and Dt / Chl a (D) versus E/K_E at 0°C (circles) and 5°C (triangles). In C an insert shows an enlargement of low irradiances. Each data point is the mean of 3 cultures measured each day during 3 consecutive days (23, 50, 80, 150, 400 μmol photon m^-2 s^-1) or 2 days (10 μmol photon m^-2 s^-1). Error bars represent standard deviations.

Fig 5

E_K^C versus E_K^ETR (A), E_K^O₂ versus E_K^ETR (B) and E_K^C versus E_K^O₂ (C) at 0°C (circles) and 5°C (triangles). In A, B, C, the dotted lines represent the 1:1 line. The growth irradiance at which growth rate (μ), carbon fixation (¹⁴C), O₂ net production, ETR and NPQ saturate (E = E_Kⁱ) is presented in D at 0°C (white bars) and 5°C (grey bars). In D, horizontal lines indicate growth irradiances (10, 23, 50, 80, 150, 400 μmol photon m^-2 s^-1).