Ultraviolet stress delays chromosome replication in light/dark synchronized cells of the marine cyanobacterium Prochlorococcus marinus PCC9511.
BACKGROUND
The marine cyanobacterium Prochlorococcus is very abundant in warm, nutrient-poor oceanic areas. The upper mixed layer of oceans is populated by high light-adapted Prochlorococcus ecotypes, which despite their tiny genome (approximately 1.7 Mb) seem to have developed efficient strategies to cope with stressful levels of photosynthetically active and ultraviolet (UV) radiation. At a molecular level, little is known yet about how such minimalist microorganisms manage to sustain high growth rates and avoid potentially detrimental, UV-induced mutations to their DNA. To address this question, we studied the cell cycle dynamics of P. marinus PCC9511 cells grown under high fluxes of visible light in the presence or absence of UV radiation. Near natural light-dark cycles of both light sources were obtained using a custom-designed illumination system (cyclostat). Expression patterns of key DNA synthesis and repair, cell division, and clock genes were analyzed in order to decipher molecular mechanisms of adaptation to UV radiation.


RESULTS
The cell cycle of P. marinus PCC9511 was strongly synchronized by the day-night cycle. The most conspicuous response of cells to UV radiation was a delay in chromosome replication, with a peak of DNA synthesis shifted about 2 h into the dark period. This delay was seemingly linked to a strong downregulation of genes governing DNA replication (dnaA) and cell division (ftsZ, sepF), whereas most genes involved in DNA repair (such as recA, phrA, uvrA, ruvC, umuC) were already activated under high visible light and their expression levels were only slightly affected by additional UV exposure.


CONCLUSIONS
Prochlorococcus cells modified the timing of the S phase in response to UV exposure, therefore reducing the risk that mutations would occur during this particularly sensitive stage of the cell cycle. We identified several possible explanations for the observed timeshift. Among these, the sharp decrease in transcript levels of the dnaA gene, encoding the DNA replication initiator protein, is sufficient by itself to explain this response, since DNA synthesis starts only when the cellular concentration of DnaA reaches a critical threshold. However, the observed response likely results from a more complex combination of UV-altered biological processes.
Kolowrat
Christian
C
UPMC-Université Paris 06, Station Biologique, Place Georges Teissier, Roscoff, France.
Partensky
Frédéric
F
Mella-Flores
Daniella
D
Le Corguillé
Gildas
G
Boutte
Christophe
C
Blot
Nicolas
N
Ratin
Morgane
M
Ferréol
Martial
M
Lecomte
Xavier
X
Gourvil
Priscillia
P
Lennon
Jean-François
JF
Kehoe
David M
DM
Garczarek
Laurence
L
D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D002453:Cell Cycle / Q000528:radiation effects; D002876:Chromosomes, Bacterial / Q000235:genetics*; D004261:DNA Replication / Q000528:radiation effects*; D015964:Gene Expression Regulation, Bacterial / Q000528:radiation effects; D017440:Photoperiod; D048929:Prochlorococcus / Q000166:cytology / Q000235:genetics* / Q000378:metabolism / Q000528:radiation effects*; D012623:Seawater / Q000382:microbiology*; D014466:Ultraviolet Rays
D001426:Bacterial Proteins