Effect of Temperature on Photosynthesis and Growth in Marine Synechococcus spp.

In this study, we develop a mechanistic understanding of how temperature affects growth and photosynthesis in 10 geographically and physiologically diverse strains of Synechococcus spp. We found that Synechococcus spp. are able to regulate photochemistry over a range of temperatures by using state transitions and altering the abundance of photosynthetic proteins. These strategies minimize photosystem II (PSII) photodamage by keeping the photosynthetic electron transport chain (ETC), and hence PSII reaction centers, more oxidized. At temperatures that approach the optimal growth temperature of each strain when cellular demand for reduced nicotinamide adenine dinucleotide phosphate (NADPH) is greatest, the phycobilisome (PBS) antenna associates with PSII, increasing the flux of electrons into the ETC. By contrast, under low temperature, when slow growth lowers the demand for NADPH and linear ETC declines, the PBS associates with photosystem I. This favors oxidation of PSII and potential increase in cyclic electron flow. For Synechococcus sp. WH8102, growth at higher temperatures led to an increase in the abundance of PBS pigment proteins, as well as higher abundance of subunits of the PSII, photosystem I, and cytochrome b6f complexes. This would allow cells to increase photosynthetic electron flux to meet the metabolic requirement for NADPH during rapid growth. These PBS-based temperature acclimation strategies may underlie the larger geographic range of this group relative to Prochlorococcus spp., which lack a PBS.Marine picocyanobacteria are the most abundant phytoplankton, inhabiting nearly every area of the surface ocean and dominating in tropical and subtropical waters. The smallest and most abundant marine picocyanobacteria belong to the genera Synechococcus and Prochlorococcus, which together account for one-third of the total primary production on Earth (Partensky et al., 1999b). Marine Synechococcus spp. are genetically diverse (Scanlan et al., 2009; Mazard et al., 2012), play an important role in the biogeochemical cycling of carbon (Grob et al., 2007), and are found from the equator to the polar circle, though they are less abundant at higher latitudes (Agusti, 2004; Scanlan et al., 2009; Huang et al., 2012). Temperature is a major factor that controls photosynthetic rates, and the biogeography of Synechococcus spp. strains in the modern ocean has been linked to temperature (Zwirglmaier et al., 2008). In this study, we explore the effect of temperature on growth and photosynthesis in several Synechococcus spp. strains.Photosynthetic electron transport in cyanobacteria, including Synechococcus spp., shares similarities with that of plants and green algae (Fig. 1). Photosynthetic organisms are commonly able to perform photosynthesis efficiently over a range of temperatures bracketing the optimal growth temperature (T_opt). However, decreased metabolic rates at temperatures too far below T_opt can cause an imbalance between photochemistry and metabolism, leading to photodamage (Huner et al., 1996). By contrast, elevated temperatures may affect membrane fluidity and denature proteins, which can also lead to a decline in photosynthetic efficiency (Falk et al., 1996). A range of diverse acclimation strategies have evolved among algae and plants to balance electron flow through the electron transport chain (ETC) during temperature fluctuations (Maxwell et al., 1994; Krol et al., 1997; Gray et al., 1998; Miśkiewicz et al., 2000).Open in a separate windowFigure 1.PBS structure and linear photosynthetic electron flow in cyanobacteria. In this schematic, the PBS is in “state 1,” indicating it is associated with a PSII dimer. Photosynthetic electron flow pathways are indicated by black arrows, and chemical reactions are indicated by blue arrows. Major ETC components include PSII, PSI, PQ/plastoquinol (PQH₂), cytochrome b6f (Cyt b6f), plastocyanin (PLC), ferredoxin (FX), flavodoxin (FL), and ferredoxin/flavodoxin NADP reductase (FNR). Other proteins depicted include the phycobiliproteins APC, PC, two forms of PE (PE I and PE II), PSII chlorophyll-binding proteins CP47 and CP43, the PSII core polypeptides D1 and D2, the PSI chlorophyll-binding core proteins PsaA and PsaB, and the PSI reaction center subunit PsaD. [See online article for color version of this figure.]Less is known about mechanisms marine cyanobacteria use to acclimate to temperature. Cyanobacteria differ from plants and green algae in that photosynthesis and respiration occur in the same membrane. In addition, the ratios of PSII:PSI are more variable in cyanobacteria (Campbell et al., 1998; Bailey et al., 2008), which can impact the flow of electrons through the ETC. Cells must prevent overreduction of the ETC because this can lead to damage of the D1 polypeptide of PSII in a process called photoinhibition; to sustain PSII activity, replacement of the damaged D1 by de novo protein synthesis is required (Aro et al., 1993). Cyanobacteria have evolved a suite of strategies to balance electron flow in the thylakoid membrane when the cells are exposed to high light; important strategies include nonphotochemical quenching (El Bissati et al., 2000; Bailey and Grossman, 2008) and alternative electron flow pathways (Asada, 1999; Bailey et al., 2008; Mackey et al., 2008). Cyanobacteria may also selectively funnel light energy to PSII or PSI to regulate the amount of electrons entering and exiting the ETC (Campbell et al., 1998).In cyanobacteria, including Synechococcus spp., the main light-harvesting antennae are water-soluble pigment-protein complexes called phycobilisomes (PBSs; Grossman et al., 1993; Six et al., 2007). Unlike the antenna of plants and algae that are embedded within the thylakoid membrane, PBSs are located on the cytoplasmic surface of the membrane (Fig. 1). Structurally, the PBS consists of phycobiliproteins, including the PBS core allophycocyanin (APC) and lateral rods of phycocyanin (PC) and phycoerythrin (PE; Fig. 1). The PBS core has evolved together with the core genome of Synechococcus spp., whereas the rod components appear to have evolved separately through gene duplication, DNA exchange between cells, and possibly virally mediated lateral gene transfer (Six et al., 2007). Each phycobiliprotein binds chromophores called phycobilins (linear tetrapyrroles) that selectively absorb different wavelengths of green-red light, thereby extending the range of photosynthetically active radiation the cell can use beyond that of chlorophyll (Campbell et al., 1998). The PBS is capable of rapid diffusion over the thylakoid membrane surface (Mullineaux et al., 1997), where it can associate with either PSI or PSII. The PBS is a mobile antenna element that does not bind chlorophyll and that likely associates with reaction centers by weak interactions with lipid head groups (Sarcina et al., 2001).State transitions, the movements of PBS or other antenna pigments between reaction centers, allow the cells to avoid PSII photodamage by balancing electron flow such that electrons do not accumulate within the ETC. Whether the PBS associates with PSI or PSII is determined by the redox poise of the plastoquinone (PQ) pool (Fig. 1), which serves as an indicator of electron flow through the ETC. When the PQ pool is oxidized, the PBS becomes associated with PSII (state 1) such that the rate of linear electron flow increases. By contrast, a reduced PQ pool elicits affiliation of the PBS with PSI (state 2), which could increase the withdrawal of electrons from the ETC. In the dark, the PQ pool tends to be reduced due to respiratory electron flow, and the PBS affiliates primarily with PSI.Recent ocean basin scale research has shed light on the role of temperature on the global distributions of Synechococcus spp. in the ocean. Collectively, these studies have shown that marine Synechococcus spp. tolerate a broad range of temperatures, likely due to high genetic diversity among strains. For example, of the four clades that dominate in natural communities, clades I and IV typically inhabit cooler waters north of 30°N and south of 30°S (Brown et al., 2005; Zwirglmaier et al., 2007, 2008), while clades II and III generally inhabit warmer tropical and subtropical waters (Fuller et al., 2006; Zwirglmaier et al., 2008). Other Synechococcus spp. sequences have been recently identified from colder waters in the northern Bering Sea and Chukchi Sea, suggesting that a possible cold adaptation could exist in some strains present at high latitudes (Huang et al., 2012). Still, other studies have found no relationship between Synechococcus spp. abundance and temperature (Zinser et al., 2007), suggesting that additional factors (e.g. nutrient availability) may be responsible for shaping Synechococcus spp. community structure (Palenik et al., 2003, 2006; Scanlan et al., 2009).While field surveys have made great strides in understanding the role of temperature in controlling picocyanobacteria distributions, much remains to be learned about the range of growth responses to temperature that can occur in marine Synechococcus spp. To date, characterization of individual Synechococcus spp. strains includes work with two isolates from the Sargasso Sea, showing variable responses to temperature (Moore et al., 1995; Fu et al., 2007). These studies demonstrate the potential for changing sea surface temperature (SST) to influence the biogeochemical role of Synechococcus spp. in the Sargasso Sea; however, little is known about whether these responses can be generalized to other strains or environments. Changes in growth rate and photosynthetic efficiency, if they occur, could alter global Synechococcus spp. distributions, affect ecosystem structure, and ultimately impact marine biogeochemical cycles and Earth’s climate, and thus could have important implications for the earth system.A mechanistic understanding of how temperature affects growth and photosynthesis in geographically and physiologically diverse strains of Synechococcus spp. is needed to clarify how temperature influences Synechococcus spp. biogeography, as well as to provide insights into how populations are likely to respond to increased SST in the future. The goal of this study is to characterize the growth, photosynthetic efficiency, and light-harvesting characteristics of 10 diverse Synechococcus spp. isolates over a range of temperatures. Using chlorophyll fluorescence analysis, we show that regulation of light harvesting via state transitions is an important acclimation process that allows cells to increase photosynthetic electron flow under high temperature conditions. This effect is enhanced for strains with higher proportions of phycoerythrobilin and phycouribilin. We use global proteome data from Synechococcus sp. WH8102 to show that this temperature-dependent enhancement is brought about in part by an increase in the abundance of PBS proteins, as well as proteins from PSII, PSI, and other ETC components. The results are discussed in the context of Synechococcus spp. biogeography in the modern ocean, and potential implications for how cells could respond to future increases in SST are considered.