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Molecular Investigation of Radiation Resistant Cyanobacterium Arthrospira Sp

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Molecular Investigation of Radiation Resistant Cyanobacterium Arthrospira Sp Molecular investigation of radiation resistant cyanobacterium Arthrospira sp. PCC8005 By Hanène Badri A dissertation presented for the degree of Doctor (PhD) in Microbiology 23rd January 2014 Jury Prof. Patrick Flammang, UMons - President Prof. David Gillan, UMons - Secretary Prof. Ruddy Wattiez, UMons - Promoter Dr. Ir. Natalie Leys, SCK•CEN - Mentor Dr. Annick Wilmotte, ULg, Belgium - External member Dr. Daniela Billi, University of Rome, Italy - External member Je dédie ce travail A la mémoire de mon cher père, pour tant de sacrifices consentis et d’encouragement. Je te dis cher père que ton rêve est réalisé, je t’envoie ce cadeau aujourd’hui tant attendu. J’ai voulu tant que tu sois présent aujourd’hui pour ma graduation, que tu sois fier de moi mais le seigneur en a décidé autrement. Paix à ton âme. A ma tendre mère qui m’a soutenu tout au long de mon chemin, avec ses encouragements A mon cher époux Salem qui m’a donné tant d’amour, tendresse et d’encouragement pendant ces dures années, on a partagé tant de moments difficiles mais aussi de joies. A vous mes frères Mohamed Taher et Mohamed Mehdi Et une spéciale dédicace pour mon futur Bébé i Abstract The cyanobacterium Arthrospira sp.PCC 8005 was selected by European Space Agency (ESA) for producing oxygen and food during future long-duration manned space missions, as part of the bioregenerative life support system 'MELiSSA'. For this task, it is essential that Arthrospira sp. PCC 8005 continues to produce oxygen and conserves high nutritive value while exposed to cosmic radiation in space. This led us to investigate in detail the tolerance and the response of Arthrospira sp. PCC 8005 to ionizing radiation. Our study showed that the Arthrospira cells are resistant to high doses of ionizing radiation, including both electromagnetic and particle irradiation. The live planktonic cells of Arthrospira sp. PCC 8005 are able to survive and fully recover their photosynthetic growth after exposure to doses of 6400 Gy of gamma irradiation, and 1000 and 2000 Gy of He and Fe particle radiation. This supports the classification of Arthrospira sp. PCC 8005 as a radiation resistant bacterium. Using a newly designed microarray chip and an optimized RNA extraction and protein analysis procedure, the molecular response of Arthrospira to high doses of gamma rays was investigated. In essence, the dynamic gene expression changes of Arthrospira sp. PCC 8005 in response to ionizing radiation over time, showed two main stages. During the early 'emergency' response, Arthrospira cells switched quickly from an active growth state to a growth arrest mode, during which the cells shut down photosynthesis and carbon fixation, and reroute their resources into cellular protection and repair. Arthrospira cells activated various antioxidant systems, such as glutathione, to detoxify the reactive oxygen species generated by the radiation, to protect essential lipids, proteins and DNA from oxidation. Arthrospira cells also activated ssDNA repair systems and systems to remove damaged amino acids and nucleic acids from the cells. During recovery, the cells induced a newly discovered cluster of genes, the arh genes, coding for proteins with unknown function but which are highly and specifically expressed in response to radiation, in a dose dependent manner. Finally, the cells restarted the vital energy and metabolic pathways, and full recover of photosynthetic proliferation could be obtained. These results, confirm that Arthrospira sp. PCC 8005 is valuable candidate for biotechnological applications in environments exposed to ionizing radiation, in space and on Earth. ii Table of contents Abstract ............................................................................................................................................ii Table of contents ............................................................................................................................ iii List of figures ................................................................................................................................... x List of tables .................................................................................................................................. xiv List of acronyms ............................................................................................................................ xvi Chapter I Arthrospira, a pioneer cyanobacterium for life support on Earth and in Space ......... 1 I.1 Abstract .............................................................................................................................. 1 I.2 Ecology of the cyanobacterium Arthrospira ..................................................................... 1 I.3 Morphology of the cyanobacterium Arthrospira ............................................................... 2 I.4 Taxonomy of the cyanobacterium Arthrospira ................................................................. 4 I.4.1 The genus Arthrospira ................................................................................................ 4 I.4.2 The species within the genus Arthrospira .................................................................. 7 I.4.3 The origin and taxonomy of Arthrospira sp. strain PCC 8005 .................................. 9 I.5 The genome of the edible cyanobacterium Arthrsopira sp. PCC8005 ............................ 10 I.5.1 Genome sequencing ................................................................................................. 10 I.5.2 Tiling-Array Design ................................................................................................. 11 I.6 Oxygen production by Arthrospira: the photosynthesis process ..................................... 12 I.6.1 Photosynthesis measurement .................................................................................... 14 I.7 Arthrospira as food supplement ...................................................................................... 18 I.7.1 Animal consumption of Arthrospira ........................................................................ 18 I.7.2 Human consumption of Arthrospira ........................................................................ 18 I.7.3 The therapeutic effects of Arthrospira food supplements ........................................ 20 I.7.4 Radiation protection effect ....................................................................................... 22 I.8 Arthrospira to support life in space ................................................................................. 22 iii I.9 References ....................................................................................................................... 25 Chapter II Ionizing radiation ..................................................................................................... 29 II.1 Abstract ............................................................................................................................ 29 II.2 Different types of ionising radiation ................................................................................ 29 II.2.1 Ionizing radiation ..................................................................................................... 29 II.2.2 Electromagnetic waves ............................................................................................. 29 II.2.3 Particulates ............................................................................................................... 30 II.2.4 Measuring Ionising Radiation .................................................................................. 31 II.2.5 Linear Energy Transfer ............................................................................................ 31 II.3 Natural ionising radiation on Earth and in Space ............................................................ 33 II.4 Biological effects of ionizing radiation ........................................................................... 36 II.4.1 Radiation-induced production of reactive oxygen species (ROS) ........................... 37 II.4.2 Lipid peroxidation .................................................................................................... 38 II.4.3 Protein oxidation ...................................................................................................... 39 II.5 DNA damage ................................................................................................................... 39 II.6 References ....................................................................................................................... 40 Chapter III Susceptibility of cyanobacteria to ionising radiation ............................................... 42 III.1 Abstract ............................................................................................................................ 42 III.1.1 Introduction .............................................................................................................. 42 III.2 Cyanobacteria and electromagnetic waves ...................................................................... 42 III.3 Management of oxidative stress and radiation damage in cyanobacteria ....................... 43 III.4 Tolerance and response of cyanobacteria to intense VIS and UV radiation ................... 44 III.4.1 Avoidance by migration and morphological changes .............................................. 46 III.4.2 Protection by UV-absorbing molecules ..................................................................
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