JPR Advance Access originally published online on June 18, 2009
Journal of Plankton Research 2009 31(9):933-938; doi:10.1093/plankt/fbp043
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HORIZONS |
Photoheterotrophy in marine prokaryotes
National Oceanography Centre, Southampton, European Way, Southampton SO14 3ZH, UK
* CORRESPONDING AUTHOR: mvz{at}noc.soton.ac.uk
Received on April 1, 2009; accepted on May 22, 2009
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONDISCUSSIONFUNDINGREFERENCES |
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Despite considerable advances in the understanding of the various microbial photoheterotrophic mechanisms, the role of solar radiation in the metabolism of bacterioplankton in the ocean is difficult to assess. It is already apparent that rates of CO2 fixation by prokaryotic cells may be only a part of the picture. Photophosphorylation is difficult to differentiate from respiratory phosphorylation and other types of ATP synthesis. Solar energy could by-pass ATP synthesis, instead being used to generate a proton-motive force, which in turn could be directly used for cell motility or even for importing molecules into cells. In addition, photoheterotrophic prokaryotes could actively regulate intake and use of solar energy for different metabolic functions depending on the energetic demands of the cell. The factors listed above hence require consideration when solar energy input into metabolism of oceanic photoheterotrophic prokaryotes is experimentally quantified and numerically modelled.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONDISCUSSIONFUNDINGREFERENCES |
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Free-living, planktonic prokaryotes, Bacteria and Archaea, here named collectively bacterioplankton, are the most abundant organisms in the World Ocean, where they produce and respire a major part of the reduced carbon or organic matter (Li, 1994
; Kirchman, 1997; Ducklow, 2000). It is notable that well over half of these prokaryotes inhabit the thin (50–150 m thickness) surface layer (Karner et al., 2001), daily irradiated by solar rays. Considering its plentiful and regular supply to the ocean surface, it is perhaps not surprising that microorganisms inhabiting the photic layer have evolved mechanisms to absorb and use solar energy for enhancing their metabolism. The fact that only two principal types of light-harvesting (chlorophyll-based and rhodopsin-based) are known strongly suggests that microorganisms started using solar energy for photosynthesis at the very beginning of biological evolution on Earth.
Photosynthesis is a broadly defined biological process of harvesting light energy for sustaining cellular metabolism including CO2 assimilation. However, photosynthesis is more familiar in its narrower definition, a biological conversion of light energy to chemical-bond energy in the form of reduced carbon compounds (Falkowski and Raven, 2007), even more specifically as the photochemical reduction and assimilation of inorganic carbon in conjunction with photolysis of water, which yields molecular oxygen as a by-product. According to scant geochemical evidence, oxygen-producing (oxygenic) photosynthetic prokaryotes (cyanobacteria) have been living and infusing the World Ocean with oxygen for over 2.5 billion years (Summons et al., 1999; Des Marais, 2000). Owing to the global biological and geological significance of carbon reduction and oxygen generation, these aspects of oxygenic photosynthesis have received far more scientific attention than other facets and types of photosynthesis. Among plankton biogeochemists, both experimentalists and modellers, photosynthesis has become synonymous with organisms capable of the narrowest definition of photosynthesis, i.e. phytoplankton. Such a simplification inevitably leads to an assumption that phytoplankton must be photoautotrophs.
Photoautotrophy or photolithotrophy, i.e. the ability to synthesize microbial cell biomass entirely from inorganic molecules using light energy, is a fundamental strategy for independent, self-sufficient survival in the photic ocean. An opposite strategy is obligate heterotrophy, i.e. an ability to grow by deriving energy as well as biomass building blocks entirely from organic molecules dispersed in water. Because all organisms are composed of reduced carbon compounds and the majority of carbon in the ocean is oxidized, photoautotrophic microbes are in fact primary producers of reduced carbon compounds not only for themselves but also for the rest of the microbial community, i.e. heterotrophic organisms. One has to remember though, generic terms like "primary producers" were introduced to assist with biogeochemical conceptual simplifications of e.g. carbon cycling in ecosystems as well as with numerical modelling of nutrient-dependent photosynthetic fixation of CO2 and trophic transfer of carbon biomass. Delicate compromises between ecological complexity and model simplification are fundamental issues of the modelling approach (Anderson, 2005). Nevertheless, the experimental approach ought to focus on reality; phototrophic prokaryotes survive in the ocean owing to numerous metabolic processes, of which oxygenic CO2 fixation is just one.
In the present-day ocean, several unicellular planktonic prokaryotes harvest light (Table I). Aerobic oxygenic chlorophyll-containing cyanobacteria of the genera Synechococcus (Waterbury et al., 1979) and Prochlorococcus (Chisholm et al., 1988) as well as aerobic anoxygenic bacteriochlorophyll-containing bacteria (Kolber et al., 2000; Kolber et al., 2001; Beja et al., 2002) use the chlorophyll-based type of light-harvesting. Conversely, proteorhodopsin-containing bacteria (Beja et al., 2000), including the most abundant planktonic prokaryote, SAR11 alphaproteobacteria (Morris et al., 2002; Giovannoni et al., 2005a), use a rhodopsin-based type of light-harvesting. The SAR11 alphaproteobacteria and Prochlorococcus cyanobacteria numerically dominate bacterioplankton at low latitudes of the photic ocean (Partensky et al., 1999; Zubkov et al., 2000; Morris et al., 2002; Mary et al., 2006). Knowledge of the presence and abundance of light-utilizing prokaryotes in the ocean has been increasing exponentially reflecting the growing scientific interest in the microbial use of solar energy. This note aims to discuss microbial strategies of exploiting solar radiation in the photic ocean and to suggest directions for further investigation.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONDISCUSSIONFUNDINGREFERENCES |
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Photoheterotrophy is common among numerically dominant oceanic prokaryotes. Even the cyanobacterial genera Prochlorococcus and Synechococcus are capable of effective and competitive uptake of significant amounts of nitrogen-containing organic molecules, such as amino acids (Zubkov et al., 2003
; Michelou et al., 2007), at low ambient concentrations (Zubkov and Tarran, 2005) for protein synthesis. Given that the strong pressure of natural selection will eliminate redundant genes (Giovannoni et al., 2005b), it is improbable that planktonic prokaryotes still maintain and use genes which are not vital for cell survival. Therefore, a strategy of active acquisition of at least some organic molecules by photoheterotrophic cells must be energetically more beneficial than de novo synthesis of these molecules. Moreover, experimental evidence suggests that light can enhance uptake of molecules by Prochlorococcus cyanobacteria as well as by SAR11 alphaproteobacteria (Mary et al., 2008b). Because of the daily sunlight cycle, as well as cloud-dependent fluctuations in radiation, photoheterotrophs adapt to living in a variable light environment and during dark periods by storing some light energy in chemical bonds and by switching to heterotrophy.
Independent evolution of both prokaryotic bacteriorhodopsin/proteorhodopsin and bacteriochlorophyll/chlorophyll type of light absorption converged on the use of photon energy to generate an electrochemical potential gradient, mainly the proton gradient or a proton-motive force (Mitchell, 1961), from which energy can be used for photophosphorylation and chemically preserved by forming ATP. The energy stored in ATP can be used equally to power numerous metabolic processes of which photosynthetic carbon reduction is just one.
In oxygenic phototrophs, cyclic and pseudocyclic photophosphorylation (Table I) is an important source of ATP required for the photosynthetic carbon reduction cycle, for the regulation of dark photoreactions and for basic cell metabolism under light or nutrient limitation (Falkowski and Raven, 2007). A widespread oceanic unicellular diazotroph UCYN-A, which fixes nitrogen in daylight, demonstrates an advanced photoheterotrophic strategy of living in the photic ocean probably undertaking photophosphorylation using photosystem I in the absence of photosystem II and therefore without oxygen production (Zehr et al., 2008).
The above example provokes lateral thoughts that perhaps the photoheterotrophic strategy of the most abundant oceanic cyanobacteria, Prochlorococcus, could also be sophisticated. There is already evidence of light enhancement (Mary et al., 2008b) and diel periodicity (Mary et al., 2008a) of amino acid uptake by Prochlorococcus cells in addition to increased amino acid uptake by Prochlorococcus cells with depth (Zubkov et al., 2004). It is quite possible that Prochlorococcus could invest significantly more energy directly from photophosphorylation into organic nutrient acquisition in nutrient-depleted oceanic gyres, presumably at the expense of CO2 reduction (Table I). Conceivably, regulation of balancing cellular energy between organic nutrient acquisition and CO2 fixation may be an additional factor on top of temperature tolerance (Johnson et al., 2006; Zinser et al., 2007) that can drive Prochlorococcus ecotype (Moore et al., 1998; West et al., 2001; Rocap et al., 2003) selection in the photic ocean.
Cyanobacteria are not the only prokaryotes that have developed a photoheterotrophic lifestyle in the photic ocean. Phylogenetically diverse aerobic anoxygenic photoheterotrophs constitute approximately 10% of oceanic bacterioplankton (Kolber et al., 2001; Beja et al., 2002) and an even higher percentage of bacterioplankton production (Koblizek et al., 2007). They are incapable of photoautotrophy and rely on heterotrophy for more than 80% of cellular energetics (Yurkov and Csotonyi, 2009). However, the remaining percentage of energy is acquired by harvesting light to photochemically oxidise organic molecules and to re-reduce CO2. Though seemingly unproductive, such photoheterotrophy must still be energetically more efficient than "pure" heterotrophy in the photic ocean. Genomic studies show that aerobic anoxygenic photoheterotrophs lack autotrophic inorganic carbon assimilation pathways (Swingley et al., 2007), so the re-reduction of CO2 should involve enzymes that are common to organisms lacking photochemical energy conversion. These enzymes can only supply a limited range of the intermediary metabolites needed for cell growth. Hence, the ecological benefits of bacteriochlorophyll-based photoheterotrophy compared with photoheterotrophy of cyanobacteria remain to be revealed (Table I).
As an alternative to a (bacterio)chlorophyll-based light-harvesting, a photon-driven proton pumping by bacteriorhodopsin is used to produce ATP and energetically supplement respiration in a group of halophilic Archaea (Danon and Stoeckenius, 1974). This type of photoheterotrophy had been thought unique to Archaea until (proteo)rhodopsins were identified in oceanic bacterioplankton (Beja et al., 2000). Apparently, bacterioplankton cells of various phylogenetic groups contain proteorhodopsin genes (de la Torre et al., 2003; Frigaard et al., 2006; Atamna-Ismaeel et al., 2008), including cyanobacteria (Miranda et al., 2009), suggesting that lateral transfer and retention of genes encoding the proteorhodopsin-based photosynthesis is common.
The transition from heterotrophy to proteorhodopsin-based photoheterotrophy seems to represent a relatively small evolutionary step (Martinez et al., 2007). Once acquired, proteorhodopsins could be spectrally (Beja et al., 2001; Sabehi et al., 2007) and energetically modified by natural selection of mutating host cells. Drawing a parallel with the symbiotic origin of eukaryotes (Margulis, 1970), rhodopsins may be seen as prokaryotic energetic equivalents of chloroplasts and mitochondria put together, giving rhodopsin-bearers significant ecological advantages. The advantages this confers in the photic ocean remain to be experimentally shown (Table I), but physiological benefits of having proton pumping rhodopsins are exploited not exclusively by prokaryotes but by eukaryotes, for example a giant unicellular alga, Acetabularia (Tsunoda et al., 2006).
Insertion of complete proteorhodopsin gene clusters into a heterologous host, Escherichia coli, generated a fully functional proteorhodopsin photosystem that enabled photophosphorylation in recombinant cells exposed to light (Martinez et al., 2007), demonstrating similarity with bacteriorhodopsin-based photophosphorylation (Racker and Stoeckenius, 1974). Proving the importance of proteorhodopsins to cell energetics, light stimulated growth of two proteorhodopsin-containing isolates of Flavobacteria (Gomez-Consarnau et al., 2007; Gonzalez et al., 2008). In contrast, although the proteorhodopsin gene was expressed, light did not stimulate growth in Pelagibacter ubique, a representative of the ubiquitous SAR11 alphaproteobacteria (Giovannoni et al., 2005a). The latter observation is difficult to interpret. Perhaps, the studied P. ubique culture was replete with organic nutrients. Consequently, oxidative phosphorylation satisfied cell demands for energy and ATP both in the dark and light conditions. Similarly, amino acid uptake by the SAR11 dominated cluster of bacterioplankton cells was not always stimulated by light (Mary et al., 2008b). An ability to regulate the proton pump performance depending on cellular energy requirements should thus be examined in future experimental studies (Table I).
Proteorhodopsins could benefit cells in a variety of ways. A light-powered proton gradient can be directly coupled to cell energetics such as a flagella-based motility (Walter et al., 2007) or possibly active transport of molecules. These molecules, imported with the help of a photon-derived proton gradient (Konings, 2006), can be used in biosynthesis rather than in respiration for ATP generation, which is instead generated by photophosphorylation (Gonzalez et al., 2008). Nearly, all nutrients are transported in P. ubique by ATP-binding cassette transporters (Giovannoni et al., 2005b) and transport functions dominate the oceanic SAR11 metaproteome (Sowell et al., 2009). This evidence suggests a considerable energy demand of SAR11 cells for nutrient acquisition, which could be met by proteorhodopsin. However, the extent to which light-harvesting by proteorhodopsins can complement or substitute other energy sources produced by SAR11 and other bacterioplankton cells in the photic ocean remains to be quantified (Table I).
The complexity and anticipated flexibility of life strategies of photoheterotrophic prokaryotes, dominating the photic ocean, poses a question about the adequacy of applying concepts of carbon flow (or even multiple element flow) to model biogeochemical cycling in these ecosystems. Because an unknown, although considerable, proportion of light energy harvested by all types of photoheterotrophs could by-pass CO2 fixation and thus be directly channelled into cell metabolism, uptake of organic molecules and growth, element-based models would be of limited use. Alternative models, based on energy flow or protein flow, could be developed and parameterized using experimental data. Although an advantage of energy-based models is in using equivalent units for different types of cellular energetics, model parameterization is problematic because of experimental challenges in measuring energy harvesting and storage in bacterioplankton cells. In a longer perspective, a protein-based model could become a more attractive alternative because proteins constitute a major part of prokaryotic cells, and protein synthesis amalgamates considerable amounts of energy in chemical bonds. Moreover, cellular protein quantity and protein turnover can be readily determined, while amino acid sequences of proteins can be used as phylogenetic markers of cells.
Summarizing the above discussion, it is clear that the rapidly emerging variety and plasticity of microbial photoheterotrophic strategies requires much more comprehensive field investigations to fully assess the input of solar energy into the metabolism of oceanic planktonic prokaryotes.
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FUNDING |
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TOPABSTRACTINTRODUCTIONDISCUSSIONFUNDINGREFERENCES |
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This study was supported by the UK Natural Environment Research Council (NERC) through the Oceans 2025 core programmes of the National Oceanography Centre, Southampton.
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ACKNOWLEDGEMENTS |
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I am indebted to Adrian Martin and Dave Scanlan for their critical comments on earlier drafts of the paper. I thank two anonymous reviewers for their constructive comments, which improved the manuscript.
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Notes |
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Corresponding editor: William Li
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