Recovery of photosynthesis after long-term storage in the terrestrial cyanobacterium Nostoc commune
The terrestrial cyanobacterium Nostoc commune is an anhydrobiotic organism with extreme longevity. Recovery of photosynthesis by rehydration was examined using our laboratory stocks of dry N. commune thalli after long-term storage in a desiccated state. In the samples stored at room temperature for...
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| Published in | Journal of general and applied microbiology Vol. 68; no. 4; pp. 169 - 174 |
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| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
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Japan
Applied Microbiology, Molecular and Cellular Biosciences Research Foundation
01.01.2022
Japan Science and Technology Agency |
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| Online Access | Get full text |
| ISSN | 0022-1260 1349-8037 |
| DOI | 10.2323/jgam.2022.01.003 |
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| Abstract | The terrestrial cyanobacterium Nostoc commune is an anhydrobiotic organism with extreme longevity. Recovery of photosynthesis by rehydration was examined using our laboratory stocks of dry N. commune thalli after long-term storage in a desiccated state. In the samples stored at room temperature for over 8 years, photosynthetic oxygen evolution was barely detectable, whereas oxygen consumption was recovered. There was an exceptional case in which photosynthetic oxygen evolution recovered after 8 years of storage at room temperature. Both photosynthetic oxygen evolution and respiratory oxygen consumption were recovered in dry thalli stored at -20°C for over 15 years. Consistent with the recovery of photosynthetic oxygen evolution, Fv/Fm was detected in the samples stored at -20°C at levels similar to those of freshly collected N. commune colonies. Carotenoids, scytonemin and chlorophyll a appeared to be intact in the dry thalli stored at -20°C, but β-carotene was not detected in the samples stored at room temperature. α-Tocopherol was intact in the samples stored at -20°C but was degraded in the samples stored at room temperature. These results suggest that dry thalli of N. commune are capable of sustaining biological activities for a long time, although they are gradually damaged when stored at room temperature. |
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| AbstractList | The terrestrial cyanobacterium Nostoc communeis an anhydrobiotic organism with extreme longevity. Recovery of photosynthesis by rehydration was examined using our laboratory stocks of dry N. commune thalli after long-term storage in a desiccated state. In the samples stored at room temperature for over 8 years, photosynthetic oxygen evolution was barely detectable, whereas oxygen consumption was recovered. There was an exceptional case in which photosynthetic oxygen evolution recovered after 8 years of storage at room temperature. Both photosynthetic oxygen evolution and respiratory oxygen consumption were recovered in dry thalli stored at -20°C for over 15 years. Consistent with the recovery of photosynthetic oxygen evolution, Fv/Fm was detected in the samples stored at -20°C at levels similar to those of freshly collected N. commune colonies. Carotenoids, scytonemin and chlorophyll a appeared to be intact in the dry thalli stored at -20°C, but β-carotene was not detected in the samples stored at room temperature. α-Tocopherol was intact in the samples stored at -20°C but was degraded in the samples stored at room temperature. These results suggest that dry thalli of N. commune are capable of sustaining biological activities for a long time, although they are gradually damaged when stored at room temperature. The terrestrial cyanobacterium Nostoc commune is an anhydrobiotic organism with extreme longevity. Recovery of photosynthesis by rehydration was examined using our laboratory stocks of dry N. commune thalli after long-term storage in a desiccated state. In the samples stored at room temperature for over 8 years, photosynthetic oxygen evolution was barely detectable, whereas oxygen consumption was recovered. There was an exceptional case in which photosynthetic oxygen evolution recovered after 8 years of storage at room temperature. Both photosynthetic oxygen evolution and respiratory oxygen consumption were recovered in dry thalli stored at -20°C for over 15 years. Consistent with the recovery of photosynthetic oxygen evolution, Fv/Fm was detected in the samples stored at -20°C at levels similar to those of freshly collected N. commune colonies. Carotenoids, scytonemin and chlorophyll a appeared to be intact in the dry thalli stored at -20°C, but β-carotene was not detected in the samples stored at room temperature. α-Tocopherol was intact in the samples stored at -20°C but was degraded in the samples stored at room temperature. These results suggest that dry thalli of N. commune are capable of sustaining biological activities for a long time, although they are gradually damaged when stored at room temperature. |
| ArticleNumber | 2022.01.003 |
| Author | Sakamoto, Toshio Wei, Yang Yuasa, Koki Nishiyama, Yoshitaka |
| Author_xml | – sequence: 1 fullname: Yuasa, Koki organization: Present address: Fisheries Technology Institute, Japan Fisheries Research and Education Agency – sequence: 1 fullname: Wei, Yang organization: Division of Biological Sciences, Graduate School of Natural Science and Technology – sequence: 1 fullname: Nishiyama, Yoshitaka organization: Department of Biochemistry and Molecular Biology, Graduate School of Science and Engineering, Saitama University – sequence: 1 fullname: Sakamoto, Toshio organization: Division of Biological Sciences, Graduate School of Natural Science and Technology |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35598979$$D View this record in MEDLINE/PubMed |
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| References | Inoue-Sakamoto, K., Nazifi, E., Tsuji, C., Asano, T., Nishiuchi, T., Matsugo, S., Ishihara, K., Kanesaki, Y., Yoshikawa, H., and Sakamoto, T. (2018b) Characterization of mycosporine-like amino acids in the cyanobacterium Nostoc verrucosum. J. Gen. Appl. Microbiol., 64, 203-211. doi: 10.2323/jgam.2017.12.003 Yoshida, T., and Sakamoto, T. (2009) Water-stress induced trehalose accumulation and control of trehalase in the cyanobacterium Nostoc punctiforme IAM M-15. J. Gen. Appl. Microbiol., 55, 135-145. doi: 10.2323/jgam.55.135 Maeda, H., Sakuragi, Y., Bryant, D. A., and DellaPenna, D. (2005) Tocopherols protect Synechocystis sp. strain PCC 6803 from lipid peroxidation. Plant Physiol., 138, 1422-1435. doi: 10.1104/pp.105.061135 Scherer, S., Ernst, A., Chen, T.-W., and Böger, P. (1984) Rewetting of drought-resistant blue-green algae: Time course of water uptake and reappearance of respiration, photosynthesis, and nitrogen fixation. Oecologia, 62, 418-423. doi: 10.1007/BF00384277 Morsy, F. M., Kuzuha, S., Takani, Y., and Sakamoto, T. (2008) Novel thermostable glycosidases in the extracellular matrix of the terrestrial cyanobacterium Nostoc commune. J. Gen. Appl. Microbiol., 54, 243-252. doi: 10.2323/jgam.54.243 Nazifi, E., Wada, N., Yamaba, M., Asano, T., Nishiuchi, T., Matsugo, S., and Sakamoto, T. (2013) Glycosylated porphyra-334 and palythine-threonine from the terrestrial cyanobacterium Nostoc commune. Mar. Drugs, 11, 3124-3154. doi: 10.3390/md11093124 Takaichi, S., Maoka, T., and Mochimaru, M. (2009) Unique carotenoids in the terrestrial cyanobacterium Nostoc commune NIES-24: 2-Hydroxymyxol 2’-fucoside, nostoxanthin and canthaxanthin. Curr. Microbiol., 59, 413-419. doi: 10.1007/s00284-009-9453-4 Hill, D. R., Hladun, S. L., Scherer, S., and Potts, M. (1994a) Water stress proteins of Nostoc commune (Cyanobacteria) are secreted with UV-A/B-absorbing pigments and associate with 1,4-beta-D-xylanxylanohydrolase activity. J. Biol. Chem., 269, 7726-7734. doi: 10.1016/S0021-9258(17)37347-7 Ueno, M., Sae-Tang, P., Kusama, Y., Hihara, Y., Matsuda, M., Hasunuma, T., and Nishiyama, Y. (2016) Moderate heat stress stimulates repair of photosystem II during photoinhibition in Synechocystis sp. PCC 6803. Plant Cell Physiol., 57, 2417-2426. doi: 10.1093/pcp/pcw153 Wei, Y., Nishiuchi, T. and Sakamoto, T. (2021) Characterization of mycosporine-like amino acids in the edible cyanobacterium Nostoc commune (Di Pi Cai) from China. J. Gen. Appl. Microbiol., in press. doi: 10.2323/jgam.2021.03.003 Nazifi, E., Wada, N., Asano, T., Nishiuchi, T., Iwamuro, Y., Chinaka, S., Matsugo, S., and Sakamoto, T. (2015) Characterization of the chemical diversity of glycosylated mycosporine-like amino acids in the terrestrial cyanobacterium Nostoc commune. J. Photochem. Photobiol. B: Biology, 142, 154-168. doi: 10.1016/j.jphotobiol.2014.12.008 Wada, N., Sakamoto, T., and Matsugo, S. (2015) Mycosporine-like amino acids and their derivatives as natural antioxidants. Antioxidants, 4, 603-646. doi: 10.3390/antiox4030603 Cameron, R. E. (1962) Species of Nostoc vaucher occurring in the Sonoran Desert in Arizona. Trans. Amer. Microsc. Soc., 81, 379-384. doi: 10.2307/3223790 Sakamoto, T., Hashimoto, A., Yamaba, M., Wada, N., Yoshida, T., Inoue-Sakamoto, K., Nishiuchi, T., and Matsugo, S. (2019) Four chemotypes of the terrestrial cyanobacterium Nostoc commune characterized by differences in the mycosporine-like amino acids. Phycol. Res., 67, 3-11. doi: 10.1111/pre.12333 Lipman, C. B. (1941) The successful revival of Nostoc commune from a herbarium specimen eighty-seven years old. Bull. Torr. Bot. Club, 68, 664-666. doi: 10.2307/2481755 Arima, H., Horiguchi, N., Takaichi, S., Kofuji, R., Ishida, K., Wada, K., and Sakamoto, T. (2012) Molecular genetic and chemotaxonomic characterization of the terrestrial cyanobacterium Nostoc commune and its neighboring species. FEMS Microbiol. Ecol., 79, 35-45. doi: 10.1111/j.1574-6941.2011.01195.x Sakamoto, T., Kumihashi, K., Kunita, S., Masaura, T., Inoue-Sakamoto, K., and Yamaguchi, M. (2011) The extracellular-matrix-retaining cyanobacterium Nostoc verrucosum accumulates trehalose, but is sensitive to desiccation. FEMS Microbiol. Ecol., 77, 385-394. doi: 10.1111/j.1574-6941.2011.01114.x Dasilva, E. J., and Jensen, A. (1971) Content of α-tocopherol in some blue-green algae. Biochim. Biophys. Acta, 239, 345-347. doi: 10.1016/0005-2760(71)90180-9 Takaichi, S. and Mochimaru, M. (2007) Carotenoids and carotenogenesis in cyanobacteria: unique ketocarotenoids and carotenoid glycosides. Cell. Mol. Life Sci., 64, 2607-2619. doi: 10.1007/s00018-007-7190-z Potts, M. (2000) Nostoc. In The Ecology of Cyanobacteria, ed. by Whitton, B. A. and Potts, M., Kluwer Academic Publishers, Netherlands, pp. 465-504. doi: 10.1007/0-306-46855-7_17 Scherer, S. and Zhong, Z.-P. (1991) Desiccation independence of terrestrial Nostoc commune ecotypes (cyanobacteria). Microbiol. Ecol., 22, 271-283. https://www.jstor.org/stable/4251214 Tamaru, Y., Takani, Y., Yoshida, T., and Sakamoto, T. (2005) Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium Nostoc commune. Appl. Environ. Microbiol., 71, 7327-7333. doi: 10.1128/AEM.71.11.7327-7333.2005 Matsui, K., Nazifi, E., Kunita, S., Wada, N., Matsugo, S., and Sakamoto, T. (2011) Novel glycosylated mycosporine-like amino acids with radical scavenging activity from the cyanobacterium Nostoc commune. J. Photochem. Photobiol. B: Biology, 105, 81-89. doi: 10.1016/j.jphotobiol.2011.07.003 T., Yoshida, T., Arima, H., Hatanaka, Y., Takani, Y., and Tamaru, Y. (2009) Accumulation of trehalose in response to desiccation and salt stress in the terrestrial cyanobacterium Nostoc commune. Phycol. Res., 57, 66-73. doi: 10.1111/j.1440-1835.2008.00522.x Fukuda, S., Yamakawa, R., Hirai, M., Kashino, Y., Koike, H., and Satoh, K. (2008) Mechanisms to avoid photoinhibition in a desiccation-tolerant cyanobacterium, Nostoc commune. Plant Cell Physiol., 49, 488-492. doi: 10.1093/pcp/pcn018 Hill, D. R., A. Peat, and M. Potts (1994b) Biochemistry and structure of the glycan secreted by desiccation-tolerant Nostoc commune (Cyanobacteria). Protoplasma, 182, 126-148. doi: 10.1007/BF01403474 DellaPenna, D. and Pogson, B. J. (2006) Vitamin synthesis in Plants: tocopherols and carotenoids. Annu. Rev. Plant Biol., 57, 711–738. doi: 10.1146/ annurev.arplant.56.032604.144301 Inoue-Sakamoto, K., Tanji, Y., Yamaba, M., Natsume, T., Masaura, T., Asano, T., Nishiuchi, T., and Sakamoto, T. (2018a) Characterization of extracellular matrix components from the desiccation-tolerant cyanobacterium Nostoc commune. J. Gen. Appl. Microbiol., 64, 15-25. doi: 10.2323/jgam.2017.03.001 Satoh, K., Hirai, M., Nishio, J., Yamaji, T., Kashino, Y., and Koike, H. (2002) Recovery of photosynthetic systems during rewetting is quite rapid in a terrestrial cyanobacterium, Nostoc commune. Plant Cell Physiol., 43, 170-176. doi: 10.1093/pcp/pcf020 Kamal-Eldin, A. and Appelqvist, L-Å. (1996) The chemistry and antioxidant properties of tocopherols and tocotrienols. Lipids, 31, 671-701. doi: 10.1007/BF02522884 Matsui, K., Nazifi, E., Hirai, Y., Wada, N., Matsugo, S., and Sakamoto, T. (2012) The cyanobacterial UV-absorbing pigment scytonemin displays radical-scavenging activity. J. Gen. App. Microbiol., 58, 137-144. doi: 10.2323/jgam.58.137 22 23 24 25 26 27 28 29 30 10 11 12 13 14 15 16 17 18 19 1 2 3 4 5 6 7 8 9 20 21 |
| References_xml | – reference: Satoh, K., Hirai, M., Nishio, J., Yamaji, T., Kashino, Y., and Koike, H. (2002) Recovery of photosynthetic systems during rewetting is quite rapid in a terrestrial cyanobacterium, Nostoc commune. Plant Cell Physiol., 43, 170-176. doi: 10.1093/pcp/pcf020 – reference: Matsui, K., Nazifi, E., Hirai, Y., Wada, N., Matsugo, S., and Sakamoto, T. (2012) The cyanobacterial UV-absorbing pigment scytonemin displays radical-scavenging activity. J. Gen. App. Microbiol., 58, 137-144. doi: 10.2323/jgam.58.137 – reference: Nazifi, E., Wada, N., Yamaba, M., Asano, T., Nishiuchi, T., Matsugo, S., and Sakamoto, T. (2013) Glycosylated porphyra-334 and palythine-threonine from the terrestrial cyanobacterium Nostoc commune. Mar. Drugs, 11, 3124-3154. doi: 10.3390/md11093124 – reference: Hill, D. R., A. Peat, and M. Potts (1994b) Biochemistry and structure of the glycan secreted by desiccation-tolerant Nostoc commune (Cyanobacteria). Protoplasma, 182, 126-148. doi: 10.1007/BF01403474 – reference: DellaPenna, D. and Pogson, B. J. (2006) Vitamin synthesis in Plants: tocopherols and carotenoids. Annu. Rev. Plant Biol., 57, 711–738. doi: 10.1146/ annurev.arplant.56.032604.144301 – reference: T., Yoshida, T., Arima, H., Hatanaka, Y., Takani, Y., and Tamaru, Y. (2009) Accumulation of trehalose in response to desiccation and salt stress in the terrestrial cyanobacterium Nostoc commune. Phycol. Res., 57, 66-73. doi: 10.1111/j.1440-1835.2008.00522.x – reference: Fukuda, S., Yamakawa, R., Hirai, M., Kashino, Y., Koike, H., and Satoh, K. (2008) Mechanisms to avoid photoinhibition in a desiccation-tolerant cyanobacterium, Nostoc commune. Plant Cell Physiol., 49, 488-492. doi: 10.1093/pcp/pcn018 – reference: Tamaru, Y., Takani, Y., Yoshida, T., and Sakamoto, T. (2005) Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium Nostoc commune. Appl. Environ. Microbiol., 71, 7327-7333. doi: 10.1128/AEM.71.11.7327-7333.2005 – reference: Matsui, K., Nazifi, E., Kunita, S., Wada, N., Matsugo, S., and Sakamoto, T. (2011) Novel glycosylated mycosporine-like amino acids with radical scavenging activity from the cyanobacterium Nostoc commune. J. Photochem. Photobiol. B: Biology, 105, 81-89. doi: 10.1016/j.jphotobiol.2011.07.003 – reference: Takaichi, S., Maoka, T., and Mochimaru, M. (2009) Unique carotenoids in the terrestrial cyanobacterium Nostoc commune NIES-24: 2-Hydroxymyxol 2’-fucoside, nostoxanthin and canthaxanthin. Curr. Microbiol., 59, 413-419. doi: 10.1007/s00284-009-9453-4 – reference: Scherer, S. and Zhong, Z.-P. (1991) Desiccation independence of terrestrial Nostoc commune ecotypes (cyanobacteria). Microbiol. Ecol., 22, 271-283. https://www.jstor.org/stable/4251214 – reference: Arima, H., Horiguchi, N., Takaichi, S., Kofuji, R., Ishida, K., Wada, K., and Sakamoto, T. (2012) Molecular genetic and chemotaxonomic characterization of the terrestrial cyanobacterium Nostoc commune and its neighboring species. FEMS Microbiol. Ecol., 79, 35-45. doi: 10.1111/j.1574-6941.2011.01195.x – reference: Nazifi, E., Wada, N., Asano, T., Nishiuchi, T., Iwamuro, Y., Chinaka, S., Matsugo, S., and Sakamoto, T. (2015) Characterization of the chemical diversity of glycosylated mycosporine-like amino acids in the terrestrial cyanobacterium Nostoc commune. J. Photochem. Photobiol. B: Biology, 142, 154-168. doi: 10.1016/j.jphotobiol.2014.12.008 – reference: Scherer, S., Ernst, A., Chen, T.-W., and Böger, P. (1984) Rewetting of drought-resistant blue-green algae: Time course of water uptake and reappearance of respiration, photosynthesis, and nitrogen fixation. Oecologia, 62, 418-423. doi: 10.1007/BF00384277 – reference: Ueno, M., Sae-Tang, P., Kusama, Y., Hihara, Y., Matsuda, M., Hasunuma, T., and Nishiyama, Y. 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Soc., 81, 379-384. doi: 10.2307/3223790 – reference: Inoue-Sakamoto, K., Tanji, Y., Yamaba, M., Natsume, T., Masaura, T., Asano, T., Nishiuchi, T., and Sakamoto, T. (2018a) Characterization of extracellular matrix components from the desiccation-tolerant cyanobacterium Nostoc commune. J. Gen. Appl. Microbiol., 64, 15-25. doi: 10.2323/jgam.2017.03.001 – reference: Dasilva, E. J., and Jensen, A. (1971) Content of α-tocopherol in some blue-green algae. Biochim. Biophys. Acta, 239, 345-347. doi: 10.1016/0005-2760(71)90180-9 – reference: Sakamoto, T., Hashimoto, A., Yamaba, M., Wada, N., Yoshida, T., Inoue-Sakamoto, K., Nishiuchi, T., and Matsugo, S. (2019) Four chemotypes of the terrestrial cyanobacterium Nostoc commune characterized by differences in the mycosporine-like amino acids. Phycol. Res., 67, 3-11. doi: 10.1111/pre.12333 – reference: Yoshida, T., and Sakamoto, T. 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| Snippet | The terrestrial cyanobacterium Nostoc commune is an anhydrobiotic organism with extreme longevity. Recovery of photosynthesis by rehydration was examined using... The terrestrial cyanobacterium Nostoc communeis an anhydrobiotic organism with extreme longevity. Recovery of photosynthesis by rehydration was examined using... |
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| SubjectTerms | anhydrobiosis antioxidant Carotene carotenoid Carotenoids Chlorophyll Cyanobacteria Desiccants desiccation tolerance Evolution Nostoc Nostoc commune Oxygen Oxygen consumption Photosynthesis Recovery Rehydration Room temperature Thalli Tocopherol Vitamin E β-Carotene |
| Title | Recovery of photosynthesis after long-term storage in the terrestrial cyanobacterium Nostoc commune |
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