Abstract
BackgroundPhotosynthetic light-harvesting proteins are the mechanism by which energy enters the marine ecosystem. The dominant prokaryotic photoautotrophs are the cyanobacterial genera Prochlorococcus and Synechococcus that are defined by two distinct light-harvesting systems, chlorophyll-bound protein complexes or phycobilin-bound protein complexes, respectively. Here, we use the Global Ocean Sampling (GOS) Project as a unique and powerful tool to analyze the environmental diversity of photosynthetic light-harvesting genes in relation to available metadata including geographical location and physical and chemical environmental parameters.MethodsAll light-harvesting gene fragments and their metadata were obtained from the GOS database, aligned using ClustalX and classified phylogenetically. Each sequence has a name indicative of its geographic location; subsequent biogeographical analysis was performed by correlating light-harvesting gene budgets for each GOS station with surface chlorophyll concentration.Conclusion/SignificanceUsing the GOS data, we have mapped the biogeography of light-harvesting genes in marine cyanobacteria on ocean-basin scales and show that an environmental gradient exists in which chlorophyll concentration is correlated to diversity of light-harvesting systems. Three functionally distinct types of light-harvesting genes are defined: (1) the phycobilisome (PBS) genes of Synechococcus; (2) the pcb genes of Prochlorococcus; and (3) the iron-stress-induced (isiA) genes present in some marine Synechococcus. At low chlorophyll concentrations, where nutrients are limited, the Pcb-type light-harvesting system shows greater genetic diversity; whereas at high chlorophyll concentrations, where nutrients are abundant, the PBS-type light-harvesting system shows higher genetic diversity. We interpret this as an environmental selection of specific photosynthetic strategy. Importantly, the unique light-harvesting system isiA is found in the iron-limited, high-nutrient low-chlorophyll region of the equatorial Pacific. This observation demonstrates the ecological importance of isiA genes in enabling marine Synechococcus to acclimate to iron limitation and suggests that the presence of this gene can be a natural biomarker for iron limitation in oceanic environments.
Highlights
In oceanic systems, oxygenic photosynthesis is performed by microbial phytoplankton, the prokaryotic component of which is dominated by two cyanobacterial genera Synechococcus spp and Prochlorococcus spp [1,2,3,4], known as oxyphotobacteria
The phylogenetic analysis of the pcb/isiA gene family from the Global Ocean Sampling (GOS) dataset (Fig. 1 and Fig. S1) resolves groups of functionally distinct genes similar to those recovered from analysis of genes in culture collections and environmental studies of the phylogeny of pcb genes [6]
The photosystem II (PSII)-type pcb genes are the most diverse group at all GOS sampling stations (Fig. 1a). This probably reflects the low chlorophyll content of PSII core dimers compared with photosystem I (PSI) core trimers [15], and the resulting need for PSII to be associated with an additional LH system to increase the functional cross-section of PSII
Summary
Oxygenic photosynthesis is performed by microbial phytoplankton, the prokaryotic component of which is dominated by two cyanobacterial genera Synechococcus spp and Prochlorococcus spp [1,2,3,4], known as oxyphotobacteria. These two genera can coexist [5]; Synechococcus are the dominant genera at temperate latitudes and coastal regions [3,4] where nutrient concentrations and biomass are relatively high, and Prochlorococcus dominate in tropical latitude ocean gyres [3,6,7,8] where nutrient concentrations and biomass are relatively low [3]. The dominant prokaryotic photoautotrophs are the cyanobacterial genera Prochlorococcus and Synechococcus that are defined by two distinct light-harvesting systems, chlorophyll-bound protein complexes or phycobilin-bound protein complexes, respectively. We use the Global Ocean Sampling (GOS) Project as a unique and powerful tool to analyze the environmental diversity of photosynthetic light-harvesting genes in relation to available metadata including geographical location and physical and chemical environmental parameters
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