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Diel rhythmicity in amino acid uptake by Prochlorococcus

Diel rhythmicity in amino acid uptake by Prochlorococcus
Diel rhythmicity in amino acid uptake by Prochlorococcus
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-synchronized 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 upregulated 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 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.

1462-2920
2124-2131
Mary, Isabelle
34d83373-e58f-452d-a9cd-2d27c908dd95
Garczarek, Laurence
547abace-863c-4448-ae9c-b2ca663d7e65
Tarran, Glen A.
218a9233-a6ae-4d0c-a9ca-35ad0d5a35f7
Kolowrat, Christian
eff0b379-2a93-4de0-aea3-572ca73f20cd
Terry, Matthew J.
a8c2cd6b-8d35-4053-8d77-3841c2427c3b
Scanlan, David J.
748c7970-2e58-4a46-82ad-0138f41bd713
Burkill, Peter H.
511b68df-1664-418f-baa1-b1075f1e1fed
Zubkov, Mikhail V.
b1dfb3a0-bcff-430c-9031-358a22b50743
Mary, Isabelle
34d83373-e58f-452d-a9cd-2d27c908dd95
Garczarek, Laurence
547abace-863c-4448-ae9c-b2ca663d7e65
Tarran, Glen A.
218a9233-a6ae-4d0c-a9ca-35ad0d5a35f7
Kolowrat, Christian
eff0b379-2a93-4de0-aea3-572ca73f20cd
Terry, Matthew J.
a8c2cd6b-8d35-4053-8d77-3841c2427c3b
Scanlan, David J.
748c7970-2e58-4a46-82ad-0138f41bd713
Burkill, Peter H.
511b68df-1664-418f-baa1-b1075f1e1fed
Zubkov, Mikhail V.
b1dfb3a0-bcff-430c-9031-358a22b50743

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, 10 (8), 2124-2131. (doi:10.1111/j.1462-2920.2008.01633.x).

Record type: Article

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-synchronized 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 upregulated 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 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.

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More information

Published date: 2008
Organisations: Biological Sciences, National Oceanography Centre,Southampton

Identifiers

Local EPrints ID: 59002
URI: http://eprints.soton.ac.uk/id/eprint/59002
ISSN: 1462-2920
PURE UUID: 6022e950-ef1a-4e0d-b471-23f7262b032e
ORCID for Matthew J. Terry: ORCID iD orcid.org/0000-0001-5002-2708

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Date deposited: 20 Aug 2008
Last modified: 16 Mar 2024 02:52

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Contributors

Author: Isabelle Mary
Author: Laurence Garczarek
Author: Glen A. Tarran
Author: Christian Kolowrat
Author: David J. Scanlan
Author: Peter H. Burkill
Author: Mikhail V. Zubkov

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