Abstract
Chlorophyll (Chl) f is the most recently discovered chlorophyll and has only been found in cyanobacteria from wet environments. Although its structure and biophysical properties are resolved, the importance of Chl f as an accessory pigment in photosynthesis remains unresolved. We found Chl f in a cyanobacterium enriched from a cavernous environment and report the first example of Chl f-supported oxygenic photosynthesis in cyanobacteria from such habitats. Pigment extraction, hyperspectral microscopy and transmission electron microscopy demonstrated the presence of Chl a and f in unicellular cyanobacteria found in enrichment cultures. Amplicon sequencing indicated that all oxygenic phototrophs were related to KC1, a Chl f-containing cyanobacterium previously isolated from an aquatic environment. Microsensor measurements on aggregates demonstrated oxygenic photosynthesis at 742 nm and less efficient photosynthesis under 768- and 777-nm light probably because of diminished overlap with the absorption spectrum of Chl f and other far-red absorbing pigments. Our findings suggest the importance of Chl f-containing cyanobacteria in terrestrial habitats.
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References
Airs RL, Temperton B, Sambles C, Farnham G, Skill SC, Llewellyn CA . (2014). Chlorophyll f and chlorophyll d are produced in the cyanobacterium Chlorogloeopsis fritschii when cultured under natural light and near-infrared radiation. FEBS Lett 588: 3770–3777.
Akutsu S, Fujinuma D, Furukawa H, Watanabe T . (2011). Pigment analysis of a chlorophyll f - containing cyanobacterium strain KC1 isolated from Lake Biwa. Photomed Photobiol 33: 35–40.
Behrendt L, Larkum A, Norman A, Qvortrup K, Chen M, Ralph P et al. (2011). Endolithic chlorophyll d-containing phototrophs. ISME J 5: 1072–1076.
Behrendt L, Larkum A, Trampe E, Norman A, Sørensen S, Kühl M . (2012). Microbial diversity of biofilm communities in microniches associated with the didemnid ascidian Lissoclinum patella. ISME J 6: 1222–1237.
Chen M, Li Y, Birch D, Willows R . (2012). A cyanobacterium that contains chlorophyll f - a red-absorbing photopigment. FEBS Lett 586: 3249–3254.
Chen M, Scheer H . (2013). Extending the limits of natural photosynthesis and implications for technical light harvesting. J Porphyrins Phthalocyanines 17: 1–15.
Chen M, Schliep M, Willows R, Cai Z-L, Neilan B, Scheer H . (2010). A red-shifted chlorophyll. Science 329: 1318–1319.
Croce R, van Amerongen H . (2014). Natural strategies for photosynthetic light harvesting. Nat Chem Biol 10: 492–501.
Gan F, Zhang S, Rockwell NC, Martin SS, Lagarias C, Bryant DA . (2014). Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345: 1312–1317.
Kühl M, Chen M, Ralph P, Schreiber U, Larkum AWD . (2005). A niche for cyanobacteria containing chlorophyll d. Nature 433: 820.
Kühl M, Polerecky L . (2008). Functional and structural imaging of phototrophic microbial communities and symbioses. Aquat Microb Ecol 53: 99–118.
Li Y, Cai Z, Chen M . (2013). Spectroscopic properties of chlorophyll f. J Phys Chem B 117: 11309–11317.
Li Y, Lin Y, Loughlin P, Chen M . (2014). Optimization and effects of different culture conditions on growth of Halomicronema hongdechloris–a filamentous cyanobacterium containing chlorophyll f. Front Plant Sci 25: 5–67.
Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S . (1996). Chlorophyll d as a major pigment. Nature 383: 402.
Miyashita H, Ohkubo S, Hirohisa K, Yuhta S, Daisuke F, Daiki F et al. (2014). Discovery of Chlorophyll d in Acaryochloris marina and Chlorophyll f in a unicellular Cyanobacterium, Strain KC1, Isolated from Lake Biwa. J Phys Chem 4: 1–9.
Revsbech N, Jorgensen B, Blackburn T, Cohen Y . (1983). Microelectrode studies of the photosynthesis and 02 H2S, and pH profiles of a microbial mat. Limnol Oceanogr 28: 1062–1074.
Stomp M, Huisman J, Stal LJ, Matthijs HCP . (2007). Colorful niches of phototrophic microorganisms shaped by vibrations of the water molecule. ISME J 1: 271–282.
Tomo T, Shinoda T, Chen M, Allakhverdiev SI, Akimoto S . (2014). Energy transfer processes in chlorophyll f-containing cyanobacteria using time-resolved fluorescence spectroscopy on intact cells. Biochim Biophys Acta 1837: 1484–1489.
Willows R, Li Y, Scheer H, Chen M . (2013). Structure of chlorophyll f. Org Lett 15: 1588–1590.
Acknowledgements
This study was supported by a grant from the Danish Research Council for Independent Research | Natural Sciences (MK). We thank Erik Trampe for assistance with high-performance liquid chromatography and hyperspectral analyses, Daniel Wangpraseurt and Milan Szabo for assistance with light measurements in the field, and Klaus Qvortrup for assistance with electron microscopy.
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Since the acceptance of this article, a survey of several cyanobacterial cultures from aquatic and terrestrial habitats has shown widespread occurrence of the ability to synthesize Chl d, Chl f, and modified phycobilins when incubated under far-red light, further corroborating our findings (Gan F, Shen G, Bryant DA. (2015). Occurrence of far-red light photoacclimation (FaRLiP) in diverse Cyanobacteria. Life 5: 4–24).
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Behrendt, L., Brejnrod, A., Schliep, M. et al. Chlorophyll f-driven photosynthesis in a cavernous cyanobacterium. ISME J 9, 2108–2111 (2015). https://doi.org/10.1038/ismej.2015.14
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DOI: https://doi.org/10.1038/ismej.2015.14
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