The acclimation response, historically known as complementary chromatic adaptation (CCA), is one process by which cyanobacterial cells use a transcriptional response to produce PBSs that are spectrally tuned to maximally absorb the prevalent wavelengths of light in the ambient environment (Gutu and Kehoe, 2012). CCA also drives light-dependent alterations of cellular or filament morphology (Bennett and Bogorad, 1973; Bordowitz and Montgomery, 2008). CCA, thus, through tuning light absorption to the external environment maximizes the potential for light energy to chemical energy conversion. Notably, CCA itself is under the regulation of a light-sensitive photosensory protein, i.e., RcaE, which controls the transcription of PBS-encoding genes (Kehoe and Grossman, 1996; Terauchi et al., 2004) and light-dependent morphological changes (Bordowitz and Montgomery, 2008; Singh and Montgomery, 2014). A mismatch between PBS protein composition with light available results in an initial loss of photosynthetic efficiency until the protein composition is recalibrated with the predominant wavelengths of light available (Campbell, 1996).

A significant contribution of energy to altering other aspects of growth and development occurs in response to changes in the external light, including morphological phenotypes. Changes in the prevalent wavelengths and intensity of light can lead to CCA-associated shifts between spherical and rod-shaped cells (Bennett and Bogorad, 1973; Bordowitz and Montgomery, 2008; Pattanaik et al., 2012; Walters et al., 2013). Distinct wavelengths have also been shown to induce cellular differentiation in some cyanobacteria from vegetative cells to other cell types including motile hormogonia (Damerval et al., 1991) or spore-like akinetes (Thompson et al., 2009). These morphological changes have largely unknown impacts on efficiency and solar energy conversion. Whereas, the ability of cells to modulate photosynthetic pigment composition is beneficial to long term culture productivity, the energetic costs or benefits of photo-dependent morphological control is less well understood. It has been suggested, however, that the morphological effects may be related to controlling cell volume and the related capacity for thylakoid membrane content, which drives PBS quantity primarily for adaptation to low light conditions (Montgomery, 2008; Pattanaik et al., 2012; Walters et al., 2013). Thus, the morphological alterations may regulate photosynthetic membrane capacity and thereby contribute to optimizing photosynthetic efficiency in response to changes in the external environment.

Similar to the benefits of regulating PBS protein or pigment composition, distinct photosystem (PS) proteins may also be used under different environmental conditions. Such alterations occur as a part of acclimation responses that are generally associated with fitness advantages under particular conditions, which include differences in light quality and/or intensity (Vinyard et al., 2013, 2014). In addition to protein substitutions or modifications, the overall antenna size may be modulated to alter cellular productivity and/or for cellular photoprotection. There are noted correlations of photosynthetic light-harvesting complex size and number with photoacclimation or photoprotection responses (Jodłowska and Latała, 2013). Diel (Jacquet et al., 2001; Poulin et al., 2014) and circadian cycles (Cervený and Nedbal, 2009) can also impact chlorophyll levels, which can be directly related to potential productivity and/or photoinhibition. Such acclimation responses suggest strong effects of growth conditions on the potential productivity of strains. These acclimation responses can either increase light-harvesting for photosynthesis or alternatively can promote photoprotection, which limits damage while often simultaneously reducing photons harvested for the photochemical reactions of photosynthesis (Figure 1).

The production of different versions of light-absorbing photosynthetic proteins or modulations of antenna size, in addition to other light-dependent changes in growth and development or photomorphogenesis, require energy that is spent during the acclimation responses – energy that is no longer available for the production of target molecules or products. To address this potential non-productive use of energy during acclimation, some analyses have been conducted to assess the benefits of truncating antennae size on supporting an overall increase in photosynthetic productivity for dense mass culturing. Truncated antennae promote light penetration and absorption for photosynthesis, while simultaneously reducing the potential for photoinhibition (reviewed by Melis, 2009).

Sigma (sig) factors that impact cyanobacterial gene transcription are themselves regulated by environmental factors (Imamura and Asayama, 2009). For example, Sig B levels increase in response to stress, including under heat shock, in response to nitrogen starvation and in darkness (for review see Imamura and Asayama, 2009). Analysis of a ΔsigB mutant in Synechocystis sp. PCC 6803 (hereafter Synechocystis) indicated that SigB serves as a negative regulator of the expression of a number of photosynthesis-related genes, among others (Foster et al., 2007). Thus, SigB accumulation under stress conditions likely contributes to downregulation of photosynthetic capacity, and thus could have a negative impact on photosynthetic capacity when overexpressed. Some cyanobacterial sigma factors also have been reported to be involved in the circadian regulation of rhythmic gene expression (Tsinoremas et al., 1996; Nair et al., 2002). The accumulation of others is regulated by light, including SigB, SigD, and SigE (Imamura et al., 2003a; Tuominen et al., 2003). These light-induced sigma factors have been shown to impact the transcription of light-induced PBS and PS genes (Imamura et al., 2003a; Summerfield and Sherman, 2007; Yoshimura et al., 2007; Pollari et al., 2009). SigB and SigD have also been shown to have a role in cellular adaptation of Synechocystis to high light conditions (Imamura et al., 2003b; Pollari et al., 2008, 2009, 2011), as has a SigD homolog in Synechococcus elongatus PCC 7942 (Seki et al., 2007). Recent studies with Synechocystis strains in which several sig genes were deleted highlighted an additional role of Sig proteins in modulating light use efficiency in response to moderate changes in light intensity (Tyystjärvi et al., 2013). Several sigma factors are, thus, directly linked to regulation of photosynthetic potential and the capacity for phototoxicity.

The correlation of several sigma factors with the regulation of photosynthesis-related genes and light use efficiency suggests that modulation of these genes could impact the development of cyanobacterial strains as production platforms. In this regard, sigB overexpression has been shown to improve the use of Synechocystis as a platform for producing the biofuel butanol, as well as for improving tolerance to non-optimal temperature and reducing reactive oxygen species (ROS) generation (Kaczmarzyk et al., 2014). By comparison, sigE overexpression negatively impacts the expression of PS genes and results in reduced photosynthetic efficiency in nutrient-replete growth (Osanai et al., 2013). Thus, the regulation of sigma factors in vivo has complex outcomes. Apart from photosynthesis-related genes, there may well be other non-photosynthetic genes whose expression is modulated by environmental regulation of sigma factors that could be vitally important for maximizing solar energy conversion and the development of cyanobacteria as biotechnological platforms. The utilization of systems biological approaches, including transcriptomics and proteomic analyses, to explore such connections could prove vitally important for further development of cyanobacterial production systems that have defined means for tuning gene expression over a wide range of conditions to promote robust and sustainable production of value target molecules.

State transitions regulate the amount of energy transferred from PBSs to the photosystems through physical movement and/or disruption of the association of the PBS with PSI or PSII at the thylakoid membrane surface (Joshua and Mullineaux, 2004). State transitions, which are defined as State 1 or 2, allow a rapid mechanism for regulating light absorption by the photosystems. In State 1, energy from PBSs is preferentially transferred to PSII; however, when light absorption exceeds the capacity of PSII excitation, a transition to State 2 occurs during which energy from PBSs is funneled to PSI (Mullineaux and Emlyn-Jones, 2005). Traditionally, lateral mobility or diffusion on the thylakoid membrane surface of PBSs between PSI and PSII reaction centers has been described as a mechanism for state transitions in cyanobacteria. Recently, a cyanobacterial megacomplex, which contains a PBS complex together with both PSI and PSII has been described (Liu et al., 2013). The megacomplex is still proposed to function to transfer energy to either PSI or PSII likely through distinct mechanisms (Liu et al., 2013). If the occurrence of this megacomplex is widespread in cyanobacteria, a revision of exactly how state transitions occur may be necessary as the need for lateral diffusion of PBS for state transitions may not be required. The coordination or control of PBS energy transfer to PSII vs. PSI is one significant point of regulation of excitation energy transfer and its conversion to chemical energy. Thus, the regulation of state transitions has the potential to drive the balance of photosynthetic energy transfer or energy dissipation for fine-tuning the conversion of chemical energy to biomass.

One mechanism for the dissipation of excess absorbed light energy depends on the function of the orange carotenoid protein (OCP) and its accessory protein fluorescence recovery protein (FRP). OCP and FRP work together to regulate energy flow from the PBS to PS in a NPQ of energy (Kirilovsky and Kerfeld, 2012, 2013). OCP is a carotenoid-bound photoactive protein that is activated by blue light (Figure 1). Photoactivated OCP binds to the PBS core and converts absorbed light energy to heat, thereby diverting energy transfer to the photosystems (Kirilovsky and Kerfeld, 2012, 2013). FRP releases activated OCP from the PBS and converts it back to its ground state, thereby resetting the system (Kirilovsky and Kerfeld, 2013). OCP has also been recently shown to have an independent role in protecting cells from strong light-induced single oxygen production, which is distinct from its role in binding to PBSs (Sedoud et al., 2014).

Another cyanobacterial photoprotective mechanism to divert potential overexcitation of the PSs involves the flavodiiron (Flv) proteins. These proteins function in removing electrons from the electron transport chain and transferring them to alternative electron acceptors (for review see Mullineaux, 2014) (Figure 1). The expression of flv genes is regulated by environmental factors including increased light intensity (Zhang et al., 2009; Bersanini et al., 2014) and fluctuating light (Allahverdiyeva et al., 2013). A greater understanding of the regulation of OCP and Flv systems may allow targeted induction of these systems to support the efficacy of cyanobacteria as biotechnological chassis.