Hot-spring bacteria reveal ability to use far-red light for photosynthesis

Fluorescence image of microcolonies of the Leptolyngbya sp. strain JSC-1 of cyanobacteria cells (JSC-1) collected from a hot spring near Yellowstone National Park. The image shows that the cells grow toward the light when light is provided only from above. Credit: Igor I. Brown, a research fellow at NASA JSC

Bacteria that grow in environments enriched in far-red light use a previously unknown process for harvesting energy. This discovery lays the foundation for further research aimed at improving plant growth and harvesting energy from the Sun, and understanding dense blooms like those now occurring on Lake Erie and other lakes worldwide. A paper describing the discovery will be published in the Science Express edition of the journal Science on 21 August 2014.

"We have shown that some cyanobacteria, also called blue-green algae, can grow in far-red wavelengths of light, a range not seen well by most humans," said Donald A. Bryant, the Ernest C. Pollard Professor of Biotechnology and a professor of biochemistry and molecular biology at Penn State. "Most cyanobacteria can't 'see' this light either. But we have found a new subgroup that can absorb and use far-red light, and we have discovered some of the surprising ways they manipulate their genes in order to grow using only these wavelengths," he said.

The scientists discovered that a cyanobacterial strain, named Leptolyngbya species strain JSC-1, completely changes its photosynthetic apparatus in order to use far-red light, which includes wavelengths longer than 700 nanometers (up to about 800 nm) -- a little longer than the range of light that most people can see. The experiments by Bryant's team revealed that these cyanobacteria replace seventeen proteins in three major light-using complexes while also making two new chlorophyll pigments that can capture the far-red light. The cells also use accessory pigments called bilins in new ways. The scientists also discovered that the organisms accomplish this feat very quickly by turning on a large number of genes to modify cellular metabolism and by simultaneously turning off a large number of other genes -- a process that they have named Far-Red Light Photoacclimation (FaRLiP).

Because the genes that are turned on, or upregulated, are the genes that determine which proteins the organism will produce, this massive remodeling of the available gene profile has a dramatic effect. "Our studies reveal that the particular cyanobacterium that we studied can extensively change its physiology and metabolism, and its photosynthetic apparatus," Bryant said. "It changes the core components of the three major photosynthetic complexes, so one ends up with a very differentiated cell that is then capable of growing in far-red light. The impact is that the organism is better than other cyanobacterial strains at producing oxygen in far-red light and, in fact, it is even better than the same cells grown under other conditions. Cells grown in far-red light produce 40 percent more oxygen when assayed in far-red light than cells grown in red light when those cells are assayed under the same far-red light conditions."

To make these discoveries, Bryant's team used a variety of biological, genetic, physical, and chemical methods in order to learn how this unusual photosynthesis apparatus works as a whole. The team's investigations included biochemical analyses, spectroscopic analyses, studies of the structures and functions of proteins, profiles of gene-transcription processes, and sequencing and comparisons of cyanobacterial genomes. "Our comparative genome-sequence analyses of different cyanobacteria strains revealed 12 additional strains that also appear to be able to use far-red light for photosynthesis," Bryant said.

This photo shows the colors of the cells of the cyanobacterium Leptolyngbya sp. strain (JSC-1), which was collected from a hot spring near Yellowstone National Park. The cells were grown in white fluorescent light (WL), green-filtered fluorescent light (GL), red light provided by 645-nm LEDs, or far-red light provided by 710-nm LEDs. Some cyanobacteria are known to appear brown when they are grown in green light and to appear blue-green when they are grown in red light, a process known as complementary chromatic acclimation. Although the cells grown in red light and far-red light look similar, research by Bryant's team showed that the photosynthetic apparatuses in these two cell types is quite different and is optimized to use light wavelengths longer than 700 nm. Credit: Fei Gan, Penn State University

The Leptolyngbya cyanobacterial strain that Bryant's team studied is one that was collected at LaDuke Hot Spring in Montana, near Yellowstone National Park. This strain was living on the underside of a mat that is so dense with bacteria that only far-red wavelengths of light penetrate to the bottom. Another environment where understanding photosynthesis in far-red light may have important implications is in the surface crusts of deserts and other soils, which cover a large percentage of Earth's surface. "It is important to understand how this photosynthetic process works in global-scale environments where cyanobacteria may be photosynthesizing with far-red light, in order to more fully understand the global impact of photosynthesis in oxygen production, carbon fixation, and other events that drive geochemical processes on our planet," Bryant said.

The research raises questions about the possibility of introducing into plants the capacity to use far-red wavelengths for photosynthesis. However, Bryant said, much more basic research is required first. "Our research already has shown that it would not be enough to insert new far-red-light-absorbing pigments into a plant unless one also has the right protein scaffolds to bind them so that they would work efficiently.  In fact, it could be quite deleterious to just start sticking long-wavelength-absorbing chlorophylls into the photosynthetic apparatus," he said.

"We now have clearly established that photosynthesis can occur in far-red light, in a wavelength range where people previously did not think that oxygenic photosynthesis could take place, and we have provided details about many of the processes involved. Now there are a whole set of associated scientific questions that need to be answered about more of the details before we can begin to investigate any applications that may or may not be possible," Bryant said. "Our research has opened up many new questions for basic scientific research."

In addition to Bryant, other members of the research team at Penn State include graduate students Fei Gan and Shuyi Zhang and University of California-Davis researchers Shelley S. Martin, Nathan Rockwell, and J. Clark Lagarias.

This study was funded by grant MCB-1021725 from the National Science Foundation to D.A.B. The genome sequence of Leptolyngbya sp. strain JSC-1 was determined under the auspices of the U.S. Department of Energy's Office of Science, Biological and Environmental Research Program, and by the University of California, Lawrence Berkeley National Laboratory under contract no. DE-AC02-05CH11231, Lawrence Livermore National Laboratory under contract no. DE-AC52-07NA27344, and Los Alamos National Laboratory under contract no. DE-AC02-06NA25396. Spectroscopic characterization of RfpA and NpR4776-PCM was funded by a grant from the Chemical Sciences, Geosciences, and Biosciences Division, Office of Basic Energy Sciences, Office of Science, U.S. Department of Energy (DOE DEFG02- 09ER16117 to J.C.L.)

CONTACTS

Donald A. Bryant: (+1) 814-777-9699, dab14@psu.edu

Barbara Kennedy (press officer): 1-814-863-4682, science@psu.edu