Micro-optics and photosynthetic light-trapping in cyanobacteria

Cyanobacteria are bacteria that grow by photosynthesis in a similar manner to plants. They are very diverse in terms of their morphology and extremely abundant in the environment: cyanobacteria in the oceans are the most abundant photosynthetic organisms on the planet and make a huge contribution to the global ecosystem. Synechocystis is a widely-used single-celled model cyanobacterium, with spherical cells about 0.003 mm in diameter. Synechocystis has the ability to move across surfaces by extending and retracting protein fibres called pili. It uses this ability to move towards light sources, and recently we investigated how such a tiny cell could be capable of detecting the position of the light source. We found that the cells act as microscopic spherical lenses, a physical property that enables them to "see" the position of a light source using the same principles that are exploited by the eyes of animals. This surprising observation prompted us to look for related effects in other cyanobacteria with different cell shapes, and we found that a cyanobacterium with elongated rod-shaped cells can trap and channel light within its elongated cell body rather like a microscopic fibre-optic. These effects appear never to have been previously considered. They are important for enabling cyanobacteria to detect the position of light sources, but they may have even more importance for photosynthesis in cyanobacteria. We envisage that photosynthesis could be influenced in several ways. Firstly, lensing effects as observed in Synechocystis could strongly concentrate light in specific regions of the cell, an effect which we think could be beneficial in low light but deleterious in high light. Secondly, fibre-optic light-trapping as observed in rod-shaped cyanobacteria could result in significantly enhanced overall light absorption by the cell. Finally, it is possible that in filamentous cyanobacteria (which consist of long chains of connected cells) the fibre-optic effect could result in light being transmitted from cell to cell, with the potential for light conduction into the interior of crowded biofilms. We think that it is essential to understand the influence of lensing and fibre-optic effects if we are to understand how cyanobacteria are able to maximise the efficiency of photosynthetic growth in the wide variety of environments that they inhabit. In this project we will measure the influence of these optical effects on photosynthesis in three model cyanobacteria: one with spherical cells, one with elongated rod-shaped cells and one with long chains of connected cells. We will quantify the influence of the optical effects on the path of light through the cells, and we will determine whether the effects are simply determined by cell size and shape, or whether they are influenced by specific features of the surface layers of the cells. We will find ways to modify the optical effects, suppressing lensing and fibre-optic trapping either by mutations that affect the cell surface layers or by immersing the cells in media whose refractive index matches that of the cell. This will enable us to quantify the influence of the optical effects on photosynthesis and allow us to determine whether the effects are beneficial or harmful in specific environments. Our results will lead to a better understanding of the growth of cyanobacteria in different environments, and we think that this could lead to a better understanding of the global ecosystem, as well as providing essential information for the efficient exploitation of cyanobacteria as solar-powered cell factories in photobioreactors.

Synechocystis is a cyanobacterium with spherical cells about 3 microns in diameter. It is capable of phototactic twitching motility. We recently investigated the basis for directional light perception in Synechocystis and made the unexpected observation that its cells act as very powerful spherical lenses, focusing a sharp image of a light source at the opposite edge of the cell. We also found that the cells of an elongated rod-shaped cyanobacterium can trap light by total internal reflection and therefore act as microscopic waveguides. These observations provided the key to understanding phototaxis in cyanobacteria, but they also have strong implications for photosynthetic performance, since micro-optic effects result in highly inhomogeneous distribution of light within the cell and also have the potential to greatly increase the optical path-length within the cell and therefore enhance the efficiency of photosynthetic light absorption. In this project we will explore the influence of micro-optic effects on photosynthesis in cyanobacteria. Since the effects are strongly dependent on the size and shape of cells we will use three model cyanobacteria: Synechocystis with spherical cells, Synechococcus with rod-shaped cells and the filamentous multicellular cyanobacterium Anabaena. In all three organisms, we will quantify the effects of lensing and internal reflection on light distribution within the cell, using the complementary techniques of fluorescence microscopy and photolithography. We will investigate whether micro-optic effects are influenced by specific features of the cyanobacterial cell surface, and we will quantify the influence of micro-optic effects on photosynthetic light absorption, photosynthetic performance and photoinhibition. The results will give a full picture of the significance of this hitherto unexplored aspect of photosynthesis, which may have implications from modelling the global ecosystem to enhancing the efficiency of photobioreactors.

The most immediate industrial beneficiaries will be biotechnological concerns interested in the exploitation of cyanobacteria for solar-powered production of biofuels and high-value products. Here, the design of efficient photobioreactors for growth of cyanobacteria (and other phototrophic micro-organisms) in mass culture is a major concern. The organisms need to be grown in dense cultures for efficient harvesting and use of space, but this can lead to very inefficient growth. For example a simple tank containing a dense culture of cyanobacteria works very inefficiently. When exposed to full sunlight, the cells in the surface layers will suffer photodamage from excess light, while cells in the interior of the tank will be shaded and suffer from light deprivation. At any one time, only a very small proportion of the culture will be in the correct light environment for efficient photosynthesis. Our preliminary results have revealed a previously unexplored aspect of the interaction of cyanobacteria with light, which will be fully characterised and quantified in our programme of research. Our research may lead to better solutions to the problem of efficient phototrophic growth in mass culture, for example by revealing adaptations that enhance photosynthesis in low light, or structures that maximise the efficiency of light absorption in cells growing within solid media or in dense biofilms. To maximise the applied potential of our research a continuous dialogue with relevant industrial concerns will be required, and the Pathways to Impact statement details plans for enabling this dialogue during the course of the project.