Current Biology Vol 18 No 8R342

Photosynthetic Pigments: PerplexingPersistent Prevalence of ‘Superfluous’Pigment Production

Phycobilins function as light-harvesting pigments in most cyanobacteria and redalgae. Although green cyanobacteria of the genus Prochlorococcus expressgenes encoding enzymes thatdirect the synthesis of phycobilins, these pigmentsdo not appear to play a role in light harvesting in Prochlorococcus. Now, it isshown that cyanophages infecting Prochlorococcus also contain genes forphycobilin-synthesizing enzymes, and these are expressed in Prochlorococcus,raising further questions as to the role of phycobilins in the host and the virus.

Samuel I. Beale

Phycobilins are accessoryphotosynthetic pigments that arefound in cyanobacteria and redalgae [1]. In their functional state,these pigments are covalentlybound to proteins calledphycobiliproteins. The latter, alongwith other, nonpigmented proteins,are organized into semisphericalarrays called phycobilisomes thatare attached to the surface of thephotosynthetic membranes — thethylakoids — which containthe photosynthetic reaction centers[2]. The energy of photons of lightabsorbed by the phycobilins istransferred to chlorophylla molecules in the reaction centersby the Forster excitation transfermechanism. The indirectlyphotoexcited chlorophyllsin the reaction centers thenundergo the photosynthetic ‘lightreaction’ — essentially aphotoionization. The phycobilisomesact as a light-absorbing antennafor photosynthesis, and are ableto efficiently absorb light in thegreen and orange spectral regionwhere chlorophyll absorbs poorly.Phycobilisomes therefore confer anadvantage to autotrophic organismsin aquatic environments, where lightin the red wavelength range, whichchlorophyll can absorb efficiently, isattenuated by water. Two majorphycobilins are phycocyanobilin,which absorbs light in the 620 nmregion, and phycoerythrobilin,which absorbs in the 560 nm region.Spectroscopic and biochemicalstudies have shown that energyfrom light absorbed byphycoerythrobilin must first betransferred to phycocyanobilinbefore it can reach chlorophyll and

contribute to photosynthesis. Thus,the presence of phycocyanobilinis necessary for phycoerythrobilinto have a light-harvestingfunction [3].

Land plants and green algaedo not have phycobilin-basedantennae. Instead, these organismsharvest light with pigment–proteincomplexes that contain chlorophyllsalong with certain carotenoids.Unlike the phycobilisomes,which are located on the surfaceof thylakoid membranes,the chlorophyll-containinglight-harvesting complexes areintegrally embedded in the thylakoidmembranes. The predominantchlorophylls of the light-harvestingcomplexes are chlorophyll a and amodified form, chlorophyll b. Thelatter is generally absent fromorganisms that use phycobilins aslight-harvesting pigments.

Several years ago an exceptionalgroup of cyanobacteria wasdiscovered that does not containphycobilisomes but, like land plantsand green algae, uses chlorophyllsa and b as its light-harvestingpigments (actually, these pigmentsare minor variants of the plantand green-algal chlorophylls, butthey function identically to them).Aside from their use of chlorophyllsinstead of phycobilins asphotosynthetic light-harvestingpigments, these organisms, namedprochlorophytes, are typicalcyanobacteria [4]. One suchprochlorophyte group, thefree-living marine Prochlorococcus,is most closely related to theSynechococcus group ofcyanobacteria. It hasrecently become evident thatProchlorococcus is responsiblefor a large portion of total

carbon fixation in marineenvironments [5].

Careful biochemical and genomicanalysis of several Prochlorococcusstrains has revealed that, eventhough they do not use phycobilinsas photosynthetic pigments, theyretain the capability to synthesizephycobilins as well as somephycobiliproteins [6–9]. In thesestrains, intact genes encodingenzymes needed for synthesisof phycoerythrobilin andphycocyanobilin from heme arepresent in the genome, andexpression of these genes inEscherichia coli yields activeenzymes. Depending on the strainand the light environment,Prochlorococcus cells also expresssome or all of these genes, andcan even covalently attachphycoerythrobilin to apoproteins toform phycoerythrin. However, thecells appear to lack genesencoding phycocyanobilin-bindingproteins. The absence of thesegenes indicates that energy fromlight absorbed by phycoerythrincannot be transferred to thephotosynthetic apparatus andthus phycoerythrin cannotcontribute to photosynthesis.Spectroscopic analysis hasconfirmed that phycoerythrincontributes very little if anythingto photosynthetic light harvestingin Prochlorococcus [10,11].

The above observations mightsuggest that the ability ofProchlorococcus to formphycobilins and phycoerythrinare vestiges carried over from anancestral phycobilisome-containingcyanobacterium and thatphycobilins have no currentphysiological role inProchlorococcus. However, thefact that the genes are expressedand the encoded biosyntheticenzymes are functional arguesagainst this interpretation. Analternative role for phycoerythrin asa storage protein seems to havebeen ruled out by observations thatphycoerythrin protein level does notdecrease in cells cultured undernitrogen deprivation [12]. In othercyanobacteria, phycobiliproteinsare degraded to serve as a sourceof nitrogen for growth undernitrogen-deficient conditions [13].A remaining possibility is that the

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bilins and/or phycoerythrin mightfunction as photosensors. Althougha photosensory role has notbeen excluded, there is noevidence to support it. Determiningthe function, if any, of phycobilinsin Prochlorococcus will ultimatelyrequire studies of theconsequences of their absence.Unfortunately, neither targetedgene disruption nor antisensesuppression has been reportedin Prochlorococcus.

The role of phycobilins inProchlorococcus has now becomemore perplexing. In a recent issue ofCurrent Biology, Dammeyer et al.[14] found that certain cyanophagesthat infect Prochlorococcus carrytheir own genes for phycobilinbiosynthesis. This finding issurprising because phages arethought to be under strong selectivepressure to keep chromosome sizeand gene content to a minimum.Nevertheless, the cyanophagesdescribed by Dammeyer et al. [14]contain genes for fully functionalphycobilin biosynthetic enzymes andthese genes are expressed inProchlorococcus. Moreover, there isa significant difference betweencyanophages and cyanobacteriain the enzymology ofphycoerythrobilin synthesis: whereascyanobacteria, includingProchlorococcus, convert biliverdinto phycoerythrobilin in two separate,two-electron reduction stepscatalyzed by two different enzymes,PebA and PebB, a cyanophage genecodes for a single enzyme, PebS,that catalyzes the entire four-electron reduction. Because thisgene is absent from allcyanobacterial genomes describedso far, it appears that the geneticbasis for phycobilin biosynthesis inthe cyanophages is not the resultof a genetic exchange with the host,but, rather, has evolvedindependently and has notundergone frequent geneticexchange with the host cells.The apparent strong positiveselection for the retention ofphycobilin-biosynthetic genes inthe cyanophages suggests thatthe ability to augment phycobilinsynthesis in their hosts confersan important advantage to thecyanophages and possiblyalso to the Prochlorococcuscells.

An alternative to the aboveinterpretation is that thecyanophages have two (or more)hosts, at least one of which isa phycobilisome-containingcyanobacterium. As a precedent,other cyanophages have beenreported to infect bothProchlorococcus andSynechococcus [15,16]. If thatwere the case for the cyanophagesdescribed by Dammeyer et al. [14],and if the genes for phycobilinand phycoerythrin synthesis conferan advantage when expressedin an alternative host, then it ispossible that these genes aresimply carried over when the hostis Prochlorococcus. Clarification ofthis interpretation will requiredetermination of the host rangeof the cyanophages and thephenotypic effects of their presencein alternative hosts.

Some lessons can be learned andsome questions are raised followingthe thought-provoking report byDammeyer et al. [14]. Firstly, weclearly don’t yet fully understandall of the roles of phycobilins incyanobacteria and, in particular, howpossession of these pigments byProchlorococcus confers competitiveor survival advantages if they do notfunction in photosynthetic lightharvesting. Secondly, given thatProchlorococcus has the ability tosynthesize phycobilins, we don’tknow what might be gained fromthe introduction of additionalphycobilin-biosynthetic machineryinto cells by the infectingcyanophages. Finally, consideringthe ability of a singlecyanophage-encoded enzyme,PebS, to convert biliverdin tophycoerythrobilin, while two enzymes,PebA and PebB, are required forthe same conversion in the hostcells, phycoerythrobilin biosynthesiscould provide an enlightening casestudy on enzyme evolution thatmight reveal the evolutionary directionfrom one enzyme to two (or viceversa) and the advantages conferredby the change.

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Division of Biology and Medicine, BrownUniversity, Providence, Rhode Island 02912,USA.E-mail: sib@brown.edu

DOI: 10.1016/j.cub.2008.02.064