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Diel rhythmicity in amino acid uptake by Prochlorococcus

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Mary, Isabelle, Garczarek, Laurence, Tarran, Glen A. , Kolowrat, Christian , Terry, Matthew J. , Scanlan, David J. , Burkill, Peter H. and Zubkov, Mikhail V. . (2008) Diel rhythmicity in amino acid uptake by Prochlorococcus. Environmental Microbiology, Vol.10 (No.8). pp. 2124-2131. ISSN 1462-2912

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Official URL: http://dx.doi.org/10.1111/j.1462-2920.2008.01633.x

Abstract

The marine cyanobacterium Prochlorococcus, the most abundant phototrophic organism on Earth, numerically dominates the phytoplankton in nitrogen (N)-depleted oceanic gyres. Alongside inorganic N sources such as nitrite and ammonium, natural populations of this genus also acquire organic N, specifically amino acids. Here, we investigated using isotopic tracer and flow cytometric cell sorting techniques whether amino acid uptake by Prochlorococcus is subject to a diel rhythmicity, and if so, whether this was linked to a specific cell cycle stage. We observed, in contrast to diurnally similar methionine uptake rates by Synechococcus cells, obvious diurnal rhythms in methionine uptake by Prochlorococcus cells in the tropical Atlantic. These rhythms were confirmed using reproducible cyclostat experiments with a light synchronised axenic Prochlorococcus (PCC9511 strain) culture and 35S-methionine and 3H-leucine tracers. Cells acquired the tracers at lower rates around dawn and higher rates around dusk despite >104 times higher concentration of ammonium in the medium, presumably because amino acids can be directly incorporated into protein. Leucine uptake rates by cells in the S+G2 cell cycle stage were consistently 2.2 times higher than those of cells at the G1 stage. Furthermore, S+G2 cells up-regulated amino acid uptake 3.5 times from dawn to dusk to boost protein synthesis prior to cell division. Because Prochlorococcus populations can account from 13% at midday, and up to 42% at dusk, of total microbial uptake of methionine and probably of other amino acids in N-depleted oceanic waters, this genus exerts diurnally variable, strong competitive pressure on other bacterioplankton populations.

Item Type:	Journal Article
Subjects:	Q Science > QL Zoology Q Science > QR Microbiology
Divisions:	Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010)
Library of Congress Subject Headings (LCSH):	Cyanobacteria, Nitrogen, Circadian rhythms
Journal or Publication Title:	Environmental Microbiology
Publisher:	Blackwell
ISSN:	1462-2912
Date:	22 April 2008
Volume:	Vol.10
Number:	No.8
Number of Pages:	8
Page Range:	pp. 2124-2131
Identification Number:	10.1111/j.1462-2920.2008.01633.x
Status:	Peer Reviewed
Access rights to Published version:	Open Access
Description:	Version accepted by publisher (post-print, after peer review, before copy-editing).
Funder:	Natural Environment Research Council (Great Britain) (NERC)
Grant number:	NE/C514723/1 (NERC)
References:	Casey, J.R., Lomas, M.W., Mandecki, J., and Walker, D.E. (2007) Prochlorococcus contributes to new production in the Sargasso Sea deep chlorophyll maximum. Geophysical Research Letters 34: doi:10.1029/2006GL028725. Chen, T.H., Chen, T.L., Hung, L.M., and Huang, T.C. (1991) Circadian-rhythm in amino acid uptake by Synechococcus RF-1. Plant Physiology 97: 55-59. Chisholm, S.W. (1992) Phytoplankton size. In Primary productivity and biogeochemical cycles in the sea. Falkowski, P.G., and Woodhead, A.D. (eds). New York: Plenum Press, pp. 213-237. Chisholm, S.W., Olson, R.J., Zettler, E.R., Goericke, R., Waterbury, J.B., and Welschmeyer, N.A. (1988) A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334: 340-343. García-Fernández, J.M., Tandeau de Marsac, N., and Diez, J. (2004) Streamlined regulation and gene loss as adaptive mechanisms in Prochlorococcus for optimised nitrogen utilization in oligotrophic environments. Microbiol Mol Biol Rev 68: 630-638. Jacquet, S. Partensky, F., Marie, D. Casotti, R., and Vaulot, D. (2001) Cell cycle regulation by light in Prochlorococcus strains. Appl Environ Microbiol 67: 782-790. Karl, D., Letelier, R., Tupas, L., Dore, J., Christian, J., and Hebel, D. (1997) The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 388: 533-538. Kettler, G.C., Martiny, A.C., Huang, K., Zucker, J., Coleman, M.L, Rodrigue, S., Chen, F., Lapidu, A., Ferriera, S., Johson, J., Steglich, C., Church, G. M. Richardson, P. and Chisholm, S.W. (2007) Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet 3: 2515-2528. Kirchman, D., and Hodson, R. (1984) Inhibition by peptides of amino acid uptake by bacterial populations in natural waters - implications for the regulation of amino acid transport and incorporation. Appl Environ Microbiol 47: 624-631. Li, W.K.W. (1994) Primary production of prochlorophytes, cyanobacteria, and eukaryotic ultraphytoplankton - measurements from flow cytometric sorting. Limnol Oceanogr 39: 169-175. Marie, D., Partensky, F., Jacquet, S., and Vaulot, D. (1997) Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl Environ Microbiol 63: 186-193. Mary, I., Tarran, G.A., Warwick, P.E., Terry, M.J., Scanlan, D.J., Burkill, P.H., and Zubkov, M.V. (2008) Light enhanced amino acid uptake by dominant bacterioplankton groups in surface waters of the Atlantic Ocean. FEMS Microbiol Ecol 63: 36–45. Montesinos, M.L., Herrero, A., and Flores, E. (1997) Amino acid transport in taxonomically diverse cyanobacteria and identification of two genes encoding elements of a neutral amino acid permease putatively involved in recapture of leaked hydrophobic amino acids. J Bacteriol 179: 853-862. Montesinos, M.L., Herrero, A., and Flores, E. (1995) Amino acid transport systems required for diazotrophic growth in the cyanobacterium Anabaena sp. strain PCC7120. J Bacteriol 177: 3150-3157. Moore L.R., Post, A.F., Rocap, G., and Chisholm, S.W. (2002) Utilisation of different nitrogen sources by the marine cyanobacteria Prochlorococcus and Synechococcus. Limnol Oceanogr 47: 989-996. Partensky, F., Hess, W.R., and Vaulot, D. (1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106-127. Pernil, R., Picossi, S., Mariscal, V., Herrero, A., and Flores, E. (2008) ABC-type amino acid uptake transporters Bgt and N-II of Anabaena sp. strain PCC 7120 share an ATPase subunit and are expressed in vegetative cells and heterocysts. Mol Microbiol doi:10.1111/j.1365-2958.2008.06107.x Picossi, S., Montesinos, M.L., Pernil, R., Lichtlé, C., Herrero, A., and Flores, E. (2005) ABC-type neutral amino acid permease N-I is required for optimal diazotrophic growth and is repressed in the heterocysts of Anabaena sp. strain PCC7120. Mol Microbiol 57: 1582-1592. Rippka, R., Coursin, T., Hess, W., Lichtle, C., Scanlan, D.J., Palinska, K.A., Iteman, I., Partensky, F., Houmard, J., and Herdman, M. (2000) Prochlorococcus marinus Chisholm et al. 1992 subsp. pastoris subsp. nov. strain PCC 9511, the first axenic chlorophyll a2/b2-containing cyanobacterium (Oxyphotobacteria). Int J Syst Evol Microbiol 50: 1833-1847. Rocap, G., Larimer, F.W., Lamerdin, J., Malfatti, S., Chain, P., Ahlgren, N.A., Arellano, A., Coleman, M., et al., (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424: 1042-1047. Rocap, G., Distel, D.L., Waterbury, J.B., and Chisholm, S.W. (2002) Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl Environ Microbiol 68: 1180-1191. Vaulot, D., Marie, D., Olson, R.J., and Chisholm, S.W. (1995) Growth of Prochlorococcus, a photosynthetic prokaryote, in the equatorial Pacific Ocean. Science 268: 1480-1482. Zubkov, M.V., and Sleigh, M.A. (2005) Assimilation efficiency of Vibrio bacterial protein biomass by the flagellate Pteridomonas: assessment using flow cytometric sorting. FEMS Microbiol Ecol 54: 281-286. Zubkov, M.V., and Tarran, G.A. (2005) Amino acid uptake of Prochlorococcus spp. in surface waters across the South Atlantic Subtropical Front. Aquat Microb Ecol 40: 241-249. Zubkov, M.V., Tarran, G.A., and Fuchs, B.M. (2004) Depth related amino acid uptake by Prochlorococcus cyanobacteria in the Southern Atlantic tropical gyre. FEMS Microbiol Ecol 50: 153-161. Zubkov, M.V., Fuchs, B.M., Tarran, G.A., Burkill, P.H., and Amann, R. (2003) High rate of uptake of organic nitrogen compounds by Prochlorococcus cyanobacteria as a key to their dominance in oligotrophic oceanic waters. Appl Environ Microbiol 69: 1299-1304. Zubkov, M.V., Mary, I., Woodward, E.M.S., Warwick, P.E., Fuchs, B.M., Scanlan, D.J., and Burkill, P.H. (2007) Microbial control of phosphate in the nutrient-depleted North Atlantic subtropical gyre. Environ Microbiol 9: 2079-2089.
URI:	http://wrap.warwick.ac.uk/id/eprint/205