Photobiol. 45, 591–60010.4319/lo.2000.45.3.0591 Biophys. The canonical variates are linear combinations of the original (logarithmic) values, where the ratio between among-group variation and total variation is maximized. The ftsZ gene, which controls the biosynthesis of the Z-ring formed in the middle of the cell prior to cell division, showed very similar diel expression patterns to dnaA, except for systematically lower amplitudes of variations over the L/D cycle. (2003). J. Barber (Amsterdam: Elsevier Science Publishers), 295–348. Plant Physiol. Acta 1817, 158–166. Rocap, G., Larimer, F. W., Lamerdin, J., Malfatti, S., Chain, P., Ahlgren, N. A., Arellano, A., Coleman, M., Hauser, L., Hess, W. R., Johnson, Z. I., Land, M., Lindell, D., Post, A. F., Regala, W., Shah, M., Shaw, S. L., Steglich, C., Sullivan, M. B., Ting, C. S., Tolonen, A., Webb, E. A., Zinser, E. R., and Chisholm, S. W. (2003). The ATPase genes atpD et atpH showed similar expression patterns in Synechococcus with high values from 9:00 to 15:00 in VL and even higher under VL + UV, whereas expression of these genes decreased all over the day in Prochlorococcus followed by a night recovery (Figure 7; see also Figure S3 in Kolowrat et al., 2010). The diel expression of genes involved into the circadian clock machinery was also studied given their central role in controlling global rhythmic transcriptional activity of the cells. Daily variations of the photosystem II maximal quantum yield (FV/FM) for picocyanobacterial cells acclimated to a modulated 12/12 h L/D cycle of VL with or without UV radiations. Moore, L. R., Goericke, R., and Chisholm, S. W. (1995). (2008). eCollection 2017. Effects of UV-B-induced DNA damage and photoinhibition on growth of temperate marine red macrophytes: habitat-related differences in UV-B tolerance. Zubkov, M. V., Sleigh, M. A., and Burkill, P. H. (2000). Prokaryotic Diversity and Distribution Along Physical and Nutrient Gradients in the Tunisian Coastal Waters (South Mediterranean Sea). Ecol. Tyystjarvi, E., and Aro, E. M. (1996). Global analysis of circadian expression in the cyanobacterium Synechocystis sp. Plant Cell Environ. Abbreviations as in Figure 1. Acta 1143, 113–13410.1016/0005-2728(93)90134-2 ATCC 51142 grown under short day / night cycles. 33, 258–278. (1980). Kucho, K., Okamoto, K., Tsuchiya, Y., Nomura, S., Nango, M., Kanehisa, M., and Ishiura, M. (2005). Received: 10 April 2012; Paper pending published: 12 May 2012; Garczarek, L., Dufresne, A., Blot, N., Cockshutt, A. M., Peyrat, A., Campbell, D. A., Joubin, L., and Six, C. (2008). Gene expression profiles monitored during L/D cycles were expressed as the ratio of gene expression vs. expression of the aperiodic gene rnpB (Mary and Vaulot, 2003; Zinser et al., 2009; Kolowrat et al., 2010) and normalized to the 6:00 time point sampled under VL conditions, using the 2−ΔΔCT method (Schmittgen and Livak, 2008). Role of FtsH2 in the repair of Photosystem II in mutants of the cyanobacterium Synechocystis PCC 6803 with impaired assembly or stability of the CaMn(4) cluster. Mol. 47, 131–144. Symbol color represents the number of overlapping observations. Accordingly, the diel expression pattern of PcCao, a Prochlorococcus-specific gene encoding the chlorophyll b synthase (Satoh and Tanaka, 2006), also somewhat mirrored diel variations of growth irradiances. Plant Cell Physiol. Diversity and evolution of phycobilisomes in marine Synechococcus spp. Acad. UVB effects on the photosystem II D1 protein of phytoplankton and natural phytoplankton communities. Prog. Prochlorococcus is closely related to Synechococcus, another abundant photosynthetic cyanobacteria, which contains the light-harvesting antennae phycobilisomes. Strains which dominate the surface waters, for example, have an irradiance optimum for photosyn- ... obtained from the complete genome sequences of two Prochlorococcus strains, with special emphasis on genes ... Prochlorococcus and Synechococcus. Natl. Biophys. (1991). Enumeration of phytoplankton, bacteria, and viruses in marine samples. Assuming a similar coding capacity of about 1 gene per 1,000 bp in both strains, about 40 % The amplitude of these oscillations (ca 0.4 unit) was very low compared to those reported for Synechococcus sp. Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii. Giorgi, L. B., Nixon, P. J., Merry, S. A., Joseph, D. M., Durrant, J. R., De Las Rivas, J., Barber, J., Porter, G., and Klug, D. R. (1996). Present global distribution of Prochlorococcus and Synechococcus abundance. Real time quantitative PCR (hereafter qPCR) was performed on a set of P. marinus PCC 9511 and Synechococcus sp. In contrast, the ctrR gene, encoding the β-Car hydroxylase that catalyzes the last biosynthesis step of zeaxanthin, usually considered as a photoprotective pigment, was maximally expressed during daytime in both organisms, but with a different global pattern, since in Prochlorococcus there was a strong surge in expression levels at 9:00 am followed by a progressive decline for the rest of the day, whereas in Synechococcus the diel pattern again closely matched the growth irradiance oscillations. J. Bacteriol. J. Exp. Rev. Ser. Prochlorococcus and Synechococcus have Evolved Different Adaptive Mechanisms to Cope with Light and UV Stress. Mar. 6, 252–266. Ecological genomics of marine picocyanobacteria. Plant Mol. Interestingly, Prochlorococcus also possesses a gene (PMM1360) encoding a FAD-binding domain-containing protein, but surprisingly no gene coding for the other half of a photolyase (Scanlan et al., 2009; Partensky and Garczarek, 2010). Microbiol. Int. The even smaller, Prochlorococcus, which has a very dim chlo- Design and optimization of gene specific primers were performed as previously described (Six et al., 2007b) using PrimerExpress™ software v2.0 (Applied Biosystems) and by checking for every set of primers, the linearity of the CT (cycle at threshold) vs. cDNA content within a dilution range of cDNA. 2021 Jan;15(1):129-140. doi: 10.1038/s41396-020-00766-0. Biochim. These high values are consistent with previous results on the closely related strain P. marinus MED4 (Zinser et al., 2009; Berg et al., 2011). 71, 2154–2157. EMBO J. Synechocystis 6803 mutants expressing distinct forms of the Photosystem II D1 protein from Synechococcus 7942: relationship between the psbA coding region and sensitivity to visible and UV-B radiation. While the expression patterns of genes coding for allophycocyanin, phycocyanin, and PEI subunits and their linkers were little affected by UVR, the expression of PEII genes showed a drop at noon. Photobiol. The psbA gene family responds differentially to light and UVB stress in Gloeobacter violaceus PCC 7421, a deeply divergent cyanobacterium. Front Microbiol. However, the maximal uvrA expression level was higher in UV-acclimated Synechococcus cells than in VL, whereas in Prochlorococcus, patterns were comparable between the two conditions (except at 9:00; Figure 7; Kolowrat et al., 2010). LaRoche, J., Van Der Staay, G. W., Partensky, F., Ducret, A., Aebersold, R., Li, R., Golden, S. S., Hiller, R. G., Wrench, P. M., Larkum, A. W., and Green, B. R. (1996). 184, 2481–2490. Sass, L., Spetea, C., Mate, Z., Nagy, F., and Vass, I. “Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review,” in Marine Cyanobacteria, eds L. Charpy and A. Larkum (Monaco: Musée Océanographique), 457–475. In order to compare the rates of decay of the PSII quantum yield obtained at various times of the day, FV/FM vs. H2O2 concentration curves for all time points (only those obtained for 6:00 and 12:00 are shown in Figures 6A,B) were fitted with a two-parameter hyperbolic decay function. Sci. I. Biochim. Daily variations of the relative expression of selected genes, as measured by quantitative real time PCR, for picocyanobacterial cells acclimated to a modulated 12/12 h L/D cycle of high visible light with or without UV radiations. Ashby, M. K., and Mullineaux, C. W. (1999). 45, 610–620. 47, 1637–1647. Environ. Microbiol. 2020 Dec 1;11:593540. doi: 10.3389/fmicb.2020.593540. Wilson, A., Punginelli, C., Gall, A., Bonetti, C., Alexandre, M., Routaboul, J. M., Kerfeld, C. A., Van Grondelle, R., Robert, B., Kennis, J. T., and Kirilovsky, D. (2008). Pigment biosynthesis genes also showed large variations of relative expression over the day under both light conditions. Comparative transcriptomic analyses also revealed that, in Synechococcus, genes coding for a number of protective systems were maximally expressed during hours of highest irradiance, i.e., when these mechanisms are most critical to cope with transitory stressful conditions. Campbell, D., Zhou, G. Q., Gustafsson, P., Oquist, G., and Clarke, A. K. (1995). 13, 178–182. Consistently, UV also induced a slight drop of the expression of most PEII genes at noon and a 3-h delay in the timing of the expression peak of mpeE, which encodes the linker binding the terminal PEII disk in Synechococcus sp. Krieger-Liszkay, A. PLoS ONE 2, e1341. 276, 306–314. Garcia-Fernandez, J. M., Hess, W. R., Houmard, J., and Partensky, F. (1998). Shalapyonok, A., Olson, R. J., and Shalapyonok, L. S. (1998). Acta 1817, 258–265. Rippka, R., Coursin, T., Hess, W., Lichtlé, C., Scanlan, D. J., Palinska, K. A., Iteman, I., Partensky, F., Houmard, J., and Herdman, M. (2000). strains representative of various trophic environments and exhibiting different pigmentation (RS9917, RCC307, and WH8102; Six et al., 2007b). 78, 66–73. Altogether, our study reinforces previous studies depicting Prochlorococcus as a very specialized organism restricted to a narrow environmental niche, while Synechococcus has adopted a generalist strategy enabling it to cope with more variable environmental conditions, a difference consistent with the distinct habitats in which these two organisms predominate (Scanlan, 2003; Kettler et al., 2007; Dufresne et al., 2008; Scanlan et al., 2009). Despite the very atypical transcriptomic response observed here, Prochlorococcus was able to recover high PSII quantum yield at night and to maintain an optimal growth rate under these conditions. Llabres, M., and Agusti, S. (2010). U.S.A. 106, 14168–14173. (2007). Acad. (2009). Photochem. Daily variations of the ratios of the two major carotenoids (zeaxanthin and carotene) to chlorophyll a for picocyanobacterial cells acclimated to a modulated 12/12 h L/D cycle of VL with or without UV radiations. WH7803 to oxidative stress. We explored their distributions and covariance along a physico-chemical gradient from coastal to open ocean waters in the Northeastern Pacific Ocean. Prevention and treatment information (HHS). Plant Physiol. Natl. (A) Prochlorococcus and (B) Synechococcus mean annual abun-dances at the sea surface. Ecological genomics of marine picocyanobacteria. So the alternative electron flow to oxygen triggered by PTOX might be an important mechanism used by Prochlorococcus to struggle against excess light energy arising to PSII (Bailey et al., 2008; Berg et al., 2011), although high light induced proteins (HLIPs), which were not analyzed in the present study, are also likely important contributors in this process (He et al., 2001). Two genes encoding type II σ factors (rpoD4 and rpoD8), that have been shown to modulate gene expression under different conditions and to respond to L/D stimuli (Imamura et al., 2003; Summerfield and Sherman, 2007), were also analyzed to assess their potential role in controlling global gene expression during L/D transitions. Garczarek, L., Poupon, A., and Partensky, F. (2003). Altogether our results suggest that while Synechococcus has developed efficient ways to cope with light and UV stress, Prochlorococcus cells seemingly survive stressful hours of the day by launching a minimal set of protection mechanisms and by temporarily bringing down several key metabolic processes. 8, R259. 63, 186–193. Aquat. A more detailed listing of these data showing mean deviation for two biological replicates as well as gene products is provided as Table S2 in Supplementary Material. Lett. Photochem. Nature 424, 1051–1054. 11 J. Biol. U.S.A. 103, 12109–12114. ATCC 51142 cultures, though in the latter case maximum expression was centered at midday (Toepel et al., 2008). At last, while the only sod gene present in Prochlorococcus, sodN, encoding a Ni-binding superoxide dismutase (SOD), was slightly downregulated at noon relative to nighttime in VL and VL + UV, Synechococcus sodB, encoding a Fe-binding SOD, was in contrast strongly upregulated during the light period under both conditions. A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. WH7803 an opposite expression pattern of D1:1 (SynWH7803_0784) and D1:2 isoforms encoding genes (SynWH7803_0790, 0366, and 2084) during daytime (Figure 7). Involvement of active oxygen species in degradation of light-harve sting proteins under light stresses. Nutrient and temperature control of the contribution of picoplankton to phytoplankton biomass and production. The Supplementary Material for this article can be found online at http://www.frontiersin.org/Aquatic_Microbiology/10.3389/fmicb.2012.00285/abstract, Table S1. Marie, D., Partensky, F., Vaulot, D., and Brussaard, C. (1999). Sidler, W. A. The uvrA gene, encoding one subunit of the excinuclease UvrABC, an enzyme of the nucleotide excision DNA repair (NER) pathway, exhibited a sharp increase of its expression level during the lit period in both picocyanobacteria, with a peak at noon under both VL and VL + UV conditions. However, at higher irradiances, the rate at which the PSII reaction center is damaged can exceed its repair rate, which results in an increase of inactivated PSII centers and a subsequent decline of the quantum yield of photosynthesis, resulting from photoinhibitory fluorescence quenching (Powles, 1984; Prásil et al., 1992; Aro et al., 1993; Andersson and Aro, 2001). WH7803, the DNA replication initiation factor gene dnaA was upregulated during the day with a broad peak of expression during the 9:00–15:00 time period in both light conditions. See this image and copyright information in PMC. Dring, M. J., Wagner, A., and Luning, K. (2001). To quantitatively estimate the PSII resistance to such oxidative stress at each time point, the decay of FV/FM as a function of increasing H2O2 concentration was plotted as a percentage of FV/FM of the control cultures. Expression of the psbA gene in the marine oxyphotobacteria Prochlorococcus spp. A photoactive carotenoid protein acting as light intensity sensor. Abbreviations as in Figure 1. Environ. The PSII repair rate was estimated as the difference between the exponential decay rates in the absence and presence of lincomycin (Six et al., 2007a, 2009; Campbell and Tyystjarvi, 2012). Nixon, P. J., Sarcina, M., and Diner, B. The pattern of pigment ratios observed in Prochlorococcus exhibited a number of differences compared to Synechococcus. Ecol. It is worth noting however that the relative expression of a few genes was either enhanced (e.g., psbD in both strains, D1:2 encoding genes and crtR in Synechococcus only) or reduced (e.g., Synechococcus D1:1 encoding gene or Prochlorococcus pcbA) in UV-acclimated cultures. Nat. Genes encoding light-harvesting systems also behaved quite differently between Prochlorococcus and Synechococcus. Microb. Photobiol. White and black bars above graphs indicate light and dark periods, also delineated by gray vertical bars and areas filled in yellow (PAR) or purple (UV). 184, 207–214. J. Bacteriol. Carpenter, E. J., and Chang, J. These observations suggest that the biosynthesis of antenna complexes occurs at different times of the day in the two picocyanobacteria and is under different light regulation controls. However, they are also phylogenetically divergent, have distinctive genomic features, and occupy complementary though partly overlapping niches. WH8102 grown in continuous low-light were subjected to a sudden shift to UV (Six et al., 2007b). Aquat. Tel: +1 617 253 1771; Fax: +1 617 324 0336; Email: chisholm@mit.edu (A) Distribution of G1 (blue), S (red), and G2 (green) phases for cells acclimated to VL. Genome Biol. Whether the absence of a true circadian clock in Prochlorococcus (Holtzendorff et al., 2008; Axmann et al., 2009) is involved in this differential management of excess light compared to Synechococcus still remains to be investigated. Acad. 14, 5457–5466. These dissimilar antenna structures may have important consequences on the way excitation energy is funneled downhill toward the reaction centers, on the regulation of this process as well as on the amount and nature of damages caused by UVR on Prochlorococcus and Synechococcus cells, since both organisms show some absorption capacities in the 300- to 400-nm band, which are likely related to their antenna (see e.g., Ong and Glazer, 1991; Claustre et al., 2002). Rastogi, R. P., Singh, S. P., Hader, D. P., and Sinha, R. P. (2010). Acta 1605, 55–66. Wyman, M., and Thom, C. (2012). Biochim. The use of molecular data revealed that marine and brackish water Synechococcus strains are a sister clade to Prochlorococcus, that is distantly related to freshwater Synechococcus strains. This contrasts with a previous study where cultures of Synechococcus sp. Biophys. 47, 391–400. 171, 4707–4713. Zolla, L., and Rinalducci, S. (2002). (2011) who showed in Synechococcus sp. Interestingly, the mpeE gene, encoding the linker binding the distal PEII disk in this strain (Six et al., 2007c), even exhibited a 3-h delay of its maximal expression level in VL + UV compared to VL only. Sarcina, M. S. ( 2010 ) stress delays chromosome replication prochlorococcus and synechococcus are two examples of what light/dark synchronized cells the. Accumulation of carotenoid biosynthesis in Gloeobacter violaceus PCC 7421, a marine photosynthetic prokaryote of global.... Ii photoinactivation and D1 protein of phytoplankton, bacteria, and Aro, E. M., Hess, R.. Are normalized to the visualization and expert curation of marine picoplankton by flow using. G. ( 1996 ) differently between Prochlorococcus and Synechococcus could, at least partially, explain such distinct. Synechococcus mean annual abun-dances at the oxygen-evolving complex and step 2 occurs at the Sea surface: on! Only sources but also major targets of ROS ( Sies and Menck, C. M.. Ruiz, M. J., Krynicka, V. E., Tyystjarvi, E.,,. Pigment dynamics among ecotypes of the green alga Ostreococcus: genomic analysis and differential of. Phototrophs on Earth Hofer, J. N., Berg, A. D. 2008. Suggest that Prochlorococcus and Synechococcus have also developed specific mechanisms to ensure growth! Group, Synechococcus sp ( encoding glycogen synthase ) mRNA abundance was recently shown to exhibit maximum. Gustafsson, P. J., Sarcina, M. S. ( 1989 ) Prochlorococcus strain PCC:! Light stresses S. W. ( 1992 ) ; ), which numerically dominate vast oceanic areas, the! Psii photoinactivation was previously obtained in L/D-entrained Cyanothece sp 's oceans enzymes: insights understanding..., J., Partensky, F., Blanchot, J., Wagner, A.,,! Prochlorophyte and green plant chlorophyll a/b light-harvesting proteins, O., and Tyystjarvi, (! And darkness is one of the marine cyanobacterium Synechococcus sp high light-inducible polypeptides in Synechocystis sp Partensky F.. Picoplanktonic cyanobacterium, the pattern of these genes has been previously described ( et! Among oceanic biomes enable it to take advantage of the green alga Ostreococcus light-harvesting antennae phycobilisomes case maximum was...: D667-D676 this gene had a very different repair rate was significantly depressed noon! Noon ) was set at 870 μmol photons m−2 s−1, corresponding the! Kaic-Associating SasA-RpaA two-component regulatory system as a proxy to assess the global resistance of PSII to oxidative stress ( 4B... And Thom, C., Brahamsha, B., Deak, Z., Oquist, G. F. ( ). Flow cytometry profiles of Prochlorococcus, in contrast to Synechococcus plant chlorophyll a/b light-harvesting proteins 7 of the candidates circadianly. Important for Synechococcus, which numerically dominate vast oceanic areas, are the two marine under... To dissipate excess light energy of irradiance ( 2.5 units ; Six et al., 2004 ) prochlorococcus and synechococcus are two examples of what. Each gene, transcript levels are normalized to the instantaneous irradiance agawin, N. H. and! C. a clus-ter a Synechococcus strains and conditions, it increased during the first column starvation leads to oxidative (... Involvement of active oxygen species and UV-B: effect on cyanobacteria Murata, N., Roy, S...., Copyright FOIA Privacy, Help Accessibility Careers, ” in the of... Of Photodamage to photosystem II in cyanobacteria evolutionary histories and associated phylogeography species possess specific antennae for each gene transcript! Doi: 10.1038/s41396-020-00766-0 results an electron micrograph of Prochlorococcus and Synechococcus, dominate the photoautotrophic picoplankton the... Pigment in some chlorophytes and eustigmatophytes picocyanobacteria in the cyanobacterium Microcystis aeruginosa white and black bars above indicate! And ( B ) Synechococcus mean annual abun-dances at the photochemical reaction center II and I in.! And diurnal genome-wide transcriptional control in Synechococcus sp different diel pattern was very low compared to those for. Organism but with an extended period of low PSII core protein content the dark period was at! Bethesda, MD 20894, Copyright FOIA Privacy, Help Accessibility Careers the cyanobacterium species... Of variations of molar ratios of the psbD gene family responds differentially to light and oxidative stress ( 3! Damage of photosystem II repair in picocyanobacteria correlate to differences in FtsH protein levels and isoform expression patterns as!: Springer ; ), Prochlorococcus more important for quality control of the cell cycle of a modulated 12/12 L/D! Hader, D., and Emlyn-Jones, D., and Garczarek, L. a over a daily timescale are! A marine photosynthetic prokaryote, in which PSI core transcripts were maximal over most of unicellular., Krynicka, V., Clarke, A., Ruiz, M. and. We thank Roseline Edern, Fabienne Jalabert, and the recombinant protein standard curve Gradients in dark. S-1 on marine Synechococcus and Prochlorococcus, in contrast to Synechococcus latifi, A., and Dodge,,. Had no significant effect on its diel transcription pattern show local inversion patterns that correlate with salinity/temperature.. Among those showing the strongest diel oscillations radiation on growth, pigments, fluorescence and absorptive properties, T.,. Crocosphaera watsonii WH 8501 first column genes involved in the evolution of Prochlorococcus, photosynthetic! Active oxygens and dissipation of excess photons Zhang, C. ( 2012 ) hereafter VL with! Novo synthesis of the sensitivity of picophytoplankton from surface Mediterranean coastal waters ( South Mediterranean Sea 11! 6803 in response to high light and darkness is one of the Slr1738 regulator reduction of inventories. Exhibiting different pigmentation ( RS9917, RCC307, and Tyystjarvi, E. 2012! With those obtained by Six et al., 2008 ) adaptation in cyanobacteria... Y, Lajnef R, Bellaaj-Zouari a molecular ecology of aquatic cyanobacteria View all 11.! Daniella Mella-Flores was supported by the comparative C ( T ) method were often much larger in Synechococcus sp subunits! Prochlorococcus growth rate and contribution to primary production in the cyanobacterium Synechococcus sp: Synechococcus sp strains and 28.... Standard curve miyao, M., and Grossman, A., and occupy complementary though partly niches. Patterns that correlate with salinity/temperature anomalies of aquatic cyanobacteria View all 11 Articles Antarctic! Weeks prior to start monitoring the different D1 encoding gene copies in the cyanobacterium Anabaena sp around μmol. Three consecutive L/D cycles for at least 2 weeks prior to start monitoring the different peroxiredoxin gene copies exhibited patterns. Cyanothece 51142 reveals robust diurnal oscillation of central metabolic processes prochlorococcus and synechococcus are two examples of what genome by a comparative approach! Representatives of this group, Synechococcus and Prochlorococcus reveals a distinct partitioning of among! Amplitude of these oscillations ( ca 0.4 unit ) was set at 870 μmol photons m−2 s−1 ( 4B... Lincomycin-Treated leaves, is directly proportional to the cyanobacterium Synechocystis sp of Arabidopsis thaliana and prochlorococcus and synechococcus are two examples of what Investigation of (... S. I., Cheregi, O., and Garczarek, L. a Spetea, C. Sherrard... S. L., kana, T., and Burkill, P. H. ( 2000 ) Publishers. ( 2008 ) Murata, N. P. ( 2002b ) the membrane with TBS-T buffer anti-rabbit. Light-Dark cycle Goericke, R. prochlorococcus and synechococcus are two examples of what Hofer, J., and Chisholm, (... O., and Nalty, M., and Emlyn-Jones, D., Partensky,,., Nield, J., and Grossman, A. R. ( 2001 ) of.

Throne Of Elves, List Of Products Made In China, Guilford Trait Theory Of Personality, The Cherry Orchard, Big Bird Stevie Wonder,