AS‐1 cyanophage infection inhibits the photosynthetic electron flow of photosystem II in <i>Synechococcus</i> sp. PCC 6301, a cyanobacterium

Teklemariam, Thomas A.; Demeter, S.; Deák, Zsuzsanna; Surányi, Gyula; Borbély, György

doi:10.1016/0014-5793(90)81270-x

Cited by 7 publications

(8 citation statements)

References 31 publications

(1 reference statement)

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“…Previous studies, prior to the genomic era and uninformed about virus-encoded photosynthesis gene products, have produced contradictory data on CO 2 fixation by cyanophage-infected freshwater cyanobacteria [22][23][24]. Therefore, in light of this realization, we revisited some of these experiments in a cyanobacterium of global importance.…”

Section: Resultsmentioning

confidence: 97%

Viruses Inhibit CO 2 Fixation in the Most Abundant Phototrophs on Earth

et al. 2016

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Marine picocyanobacteria of the genera Prochlorococcus and Synechococcus are the most numerous photosynthetic organisms on our planet [1, 2]. With a global population size of 3.6 × 10(27) [3], they are responsible for approximately 10% of global primary production [3, 4]. Viruses that infect Prochlorococcus and Synechococcus (cyanophages) can be readily isolated from ocean waters [5-7] and frequently outnumber their cyanobacterial hosts [8]. Ultimately, cyanophage-induced lysis of infected cells results in the release of fixed carbon into the dissolved organic matter pool [9]. What is less well known is the functioning of photosynthesis during the relatively long latent periods of many cyanophages [10, 11]. Remarkably, the genomes of many cyanophage isolates contain genes involved in photosynthetic electron transport (PET) [12-18] as well as central carbon metabolism [14, 15, 19, 20], suggesting that cyanophages may play an active role in photosynthesis. However, cyanophage-encoded gene products are hypothesized to maintain or even supplement PET for energy generation while sacrificing wasteful CO2 fixation during infection [17, 18, 20]. Yet this paradigm has not been rigorously tested. Here, we measured the ability of viral-infected Synechococcus cells to fix CO2 as well as maintain PET. We compared two cyanophage isolates that share different complements of PET and central carbon metabolism genes. We demonstrate cyanophage-dependent inhibition of CO2 fixation early in the infection cycle. In contrast, PET is maintained throughout infection. Our data suggest a generalized strategy among marine cyanophages to redirect photosynthesis to support phage development, which has important implications for estimates of global primary production.

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Section: Resultsmentioning

confidence: 97%

Viruses Inhibit CO 2 Fixation in the Most Abundant Phototrophs on Earth

et al. 2016

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“…Waters & Chan 1982, Suttle et al 1990, Balachandran et al 1997, Juneau et al 2003 and have revealed mechanisms that may also be applicable to natural coccolithophore populations. Typically, inhibition of photosynthesis occurs as a result of indirect viral interference with electron flow, thought to be associated with the change from host protein and nucleic acid synthesis to synthesis of virus-encoded protein and nucleic acid (Teklemariam et al 1990, Seaton et al 1995. Subsequently, there is a loss of PSII-PSI electron transport efficiency due to destabilisation of PSII-dependent protein turnover (Van Etten et al 1991), observed as a reduction in photochemical quenching and an increase in fluorescence quenching, and indicated by a decrease in darkadapted F v /F m (Teklemariam et al 1990, Seaton et al 1995, Seaton et al 1996, Balachandran et al 1997, Rahoutei et al 2000, Hewson et al 2001, Juneau et al 2003.…”

Section: Discussionmentioning

confidence: 99%

“…Several studies have investigated the changes in phytoplankton photosynthesis during viral infection (e.g. Waters & Chan 1982, Van Etten et al 1983, Teklemariam et al 1990, Suttle 1992, Suttle & Chan 1993, Juneau et al 2003) and most, but not all (Hewson et al 2001, Lindell et al 2005, have shown reduced photosynthetic activity at some point following viral enrichment. During infection of Micromonas pusilla, though photosynthesis declined only at the point of lysis, photosystems (particularly PSII complexes) were functioning with a higher biochemical turnover rate during late infection and lysis (Brown et al 2007).…”

Section: Introductionmentioning

confidence: 99%

“…Viral infection of a phytoplankton cell inevitably results in physiological consequences to the host metabolism, leading to the activation of stress and defence mechanisms (Bidle et al 2007, Vardi et al 2009), which in turn can alter growth dynamics and lifecycle (Frada et al 2008). One such consequence is a viral-induced disruption of photosynthesis, thought to be associated with a reduced efficiency of electron capture by photosystem (PS) II reaction centres from the light-harvesting pigments (Seaton et al 1995, Juneau et al 2003) and inhibition of electron transport between PSII and PSI (Teklemariam et al 1990, Seaton et al 1995, Balachandran et al 1997, potentially leading to elevated oxidative stress within cells as a result of uncontrolled singlet oxygen production (Asada 1994, Evans et al 2006. Changes in photosynthetic activity can have major implications for the physiological status of autotrophic cells, which, in turn, will have ecological and biogeochemical consequences.…”

Section: Introductionmentioning

confidence: 99%

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Reduction in photosystem II efficiency during a virus-controlled Emiliania huxleyi bloom

Kimmance¹,

Allen²,

Pagarete³

et al. 2014

Mar. Ecol. Prog. Ser.

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During viral infection of Emiliania huxleyi, laboratory studies have shown that photosystem (PS) II efficiency declines during the days post-infection and is thought to be associated with viral-induced interruption of electron transport rates between photosystems. However, measuring the impact of viral infection on PSII function in E. huxleyi populations from natural, taxo nomically diverse phytoplankton communities is difficult, and whether this phenomenon occurs in nature is presently unknown. Here, chlorophyll fluorescence analysis was used to assess changes in PSII efficiency throughout an E. huxleyi bloom during a mesocosm experiment off the coast of Norway. Specifically, we aimed to determine whether a measurable suppression of the efficiency of PSII photochemistry could be observed due to viral infection of the natural E. huxleyi populations. During the major infection period prior to bloom collapse, there was a significant reduction in PSII efficiency with an average decrease in maximum PSII photochemical efficiency (F v /F m ) of 17% and a corresponding 75% increase in maximum PSII effective absorption crosssection (σ PSII ); this was concurrent with a significant decrease in E. huxleyi growth rates and an increase in E. huxleyi virus (EhV) production. As E. huxleyi populations dominated the phytoplankton community and potentially contributed up to 100% of the chlorophyll a pool, we believe that the variable chlorophyll fluorescence signal measured during this period was derived predominantly from E. huxleyi and, thus, reflects changes occurring within E. huxleyi cells. This is the first demonstration of suppression of PSII photochemistry occurring during viral infection of natural coccolithophore populations. KEY WORDS: Viral infection · Emiliania huxleyi bloom · Chlorophyll fluorescence · Photosystem II efficiency · MesocosmResale or republication not permitted without written consent of the publisher Editorial responsibility: Katherine Richardson,

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“…However, the effect of viral infection on the photosynthetic activity of this ecologically important species has not been studied. Most studies examining photosynthetic alteration of infected phytoplankton have been conducted with cyanobacteria (Adolph & Haselkorn 1972, Allen & Hutchison 1976, Teklemariam et al 1990, Suttle & Chan 1993, but some studies have been carried out with the marine prasinophyte Micromonas pusilla and the chlorophyte Chlorella (Waters & Chan 1982, Van Etten et al 1983. In some instances viral infection leads to the immediate suppression of photosynthetic activity (Van Etten et al 1983), whereas in other cases photosynthesis continues to the point of the complete lysis of the population (Mackenzie & Haselkorn 1972, Allen & Hutchison 1976, Suttle & Chan 1993.…”

Section: Introductionmentioning

confidence: 99%

Effects of viral infection on photosynthetic processes in the bloom-forming alga Heterosigma akashiwo

Juneau¹,

Lawrence²,

Suttle³

et al. 2003

Aquat. Microb. Ecol.

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Pulse-amplitude-modulated (PAM) fluorescence is a technique that allows rapid assessment of photosynthetic activity of phytoplankton. This approach was used to evaluate the effect of viral infection on the photosynthesis of Heterosigma akashiwo, a toxic bloom-forming raphidophyte found in coastal waters of Japan and Canada. We found that viral infection caused by a single strand RNA virus (HaRNAV Strain 263) and 2 uncharacterised DNA viruses (Strains WBs1 and OIs1) gradually impaired photosynthetic activity during the lytic cycle and that photosynthetic electron transport was directly affected by viral infection. Photosystem (PS) II quantum yield of the active reaction centre was much less affected than the overall PSII-PSI electron transport. The decrease in the photosynthetic activity of the infected algae promoted the non-photochemical energy dissipation (heat). Furthermore, the lytic cycle of the viruses was of similar duration in darkness as in the light (ca. 100 h), and therefore it was not dependent on photophosphorylation. Our study demonstrates that the sensitivity of PAM fluorometry makes it a useful tool for studying viral infection in phytoplankton populations. Moreover, the results have implications for understanding the role of viral infection on the bloom dynamics of H. akashiwo by showing that viral replication is not lightdependent. Hence, viral production can occur below the photic zone. KEY WORDS: Viral infection · Photosynthetic activity · PAM chlorophyll fluorescence · Heterosigma akashiwo Resale or republication not permitted without written consent of the publisherAquat Microb Ecol 31: 9-17, 2003 Etten et al. 1983). In some instances viral infection leads to the immediate suppression of photosynthetic activity (Van Etten et al. 1983), whereas in other cases photosynthesis continues to the point of the complete lysis of the population (Mackenzie & Haselkorn 1972, Allen & Hutchison 1976, Suttle & Chan 1993. Even similar viruses can have very different effects on their hosts. For example, both M. pusilla virus (MpV) and the Chlorella virus (PBCV1) are members of the family Phycodnaviridae, but photosynthesis is altered by infection more quickly in Chlorella than in M. pusilla (Waters & Chan 1982, Van Etten et al. 1983.One relatively simple way to determine photosynthetic activity, and thus gain insight into the physiological state of plants, is by chlorophyll a (chl a) fluorescence measurement (Lichtenthaler & Rinderle 1988, Bolhàr-Nordenkampf et al. 1989. A fraction of the light energy absorbed by plants is re-emitted as chl a fluorescence, a dissipation process that is in competition with non-radiative energy dissipation processes, both photochemical and non-photochemical (for a review see Lavorel & Etienne 1977). The level of emitted fluorescence is linked to the redox state of the Photosystem II (PSII) primary electron acceptor, Q A , and plastoquinone (PQ) pool. Upon illumination, the fluorescence signal increases rapidly due to the reduction of these electron acceptors. Ther...

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AS‐1 cyanophage infection inhibits the photosynthetic electron flow of photosystem II in Synechococcus sp. PCC 6301, a cyanobacterium

Cited by 7 publications

References 31 publications

Viruses Inhibit CO 2 Fixation in the Most Abundant Phototrophs on Earth

Viruses Inhibit CO 2 Fixation in the Most Abundant Phototrophs on Earth

Reduction in photosystem II efficiency during a virus-controlled Emiliania huxleyi bloom

Effects of viral infection on photosynthetic processes in the bloom-forming alga Heterosigma akashiwo

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