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The diversity of cyanobacterial metabolism: genome analysis of multiple phototrophic microorganisms.

Beck C, Knoop H, Axmann IM, Steuer R - BMC Genomics (2012)

Bottom Line: We describe genetic diversity found within cyanobacterial genomes, specifically with respect to metabolic functionality.Our results have direct implications for resource allocation and further sequencing projects.It can be extrapolated that the number of newly identified genes still significantly increases with increasing number of new sequenced genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute for Theoretical Biology, Humboldt-University of Berlin, Invalidenstr, 43, D-10115 Berlin, Germany.

ABSTRACT

Background: Cyanobacteria are among the most abundant organisms on Earth and represent one of the oldest and most widespread clades known in modern phylogenetics. As the only known prokaryotes capable of oxygenic photosynthesis, cyanobacteria are considered to be a promising resource for renewable fuels and natural products. Our efforts to harness the sun's energy using cyanobacteria would greatly benefit from an increased understanding of the genomic diversity across multiple cyanobacterial strains. In this respect, the advent of novel sequencing techniques and the availability of several cyanobacterial genomes offers new opportunities for understanding microbial diversity and metabolic organization and evolution in diverse environments.

Results: Here, we report a whole genome comparison of multiple phototrophic cyanobacteria. We describe genetic diversity found within cyanobacterial genomes, specifically with respect to metabolic functionality. Our results are based on pair-wise comparison of protein sequences and concomitant construction of clusters of likely ortholog genes. We differentiate between core, shared and unique genes and show that the majority of genes are associated with a single genome. In contrast, genes with metabolic function are strongly overrepresented within the core genome that is common to all considered strains. The analysis of metabolic diversity within core carbon metabolism reveals parts of the metabolic networks that are highly conserved, as well as highly fragmented pathways.

Conclusions: Our results have direct implications for resource allocation and further sequencing projects. It can be extrapolated that the number of newly identified genes still significantly increases with increasing number of new sequenced genomes. Furthermore, genome analysis of multiple phototrophic strains allows us to obtain a detailed picture of metabolic diversity that can serve as a starting point for biotechnological applications and automated metabolic reconstructions.

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A pathway diagram of the cyanobacterial core metabolic network. Black boxes indicate enzymes whose corresponding CLOGs are associated with all 16 cyanobacterial strains. Grey boxes correspond to enzymes that are not annotated for one or more strains.
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Figure 8: A pathway diagram of the cyanobacterial core metabolic network. Black boxes indicate enzymes whose corresponding CLOGs are associated with all 16 cyanobacterial strains. Grey boxes correspond to enzymes that are not annotated for one or more strains.

Mentions: Beyond storage compounds, Tables 4 and 5 summarize the presence of several key enzymes within cyanobacterial central metabolism across all 16 strains considered in this study. In contrast to Table 3, the tables do not distinguish between individual CLOGs associated with the same enzymatic function. A detailed depiction of individual CLOGs is provided as supplementary material (Additional File 6). For each enzyme usually a dominant CLOG exists in addition to a smaller number of secondary CLOGs. A graphical depiction of annotated pathways is given in Figure 8. Tables 4 and 5 allow for a detailed analysis of metabolic function. First, we note that all key enzymes of the Calvin-Benson cycle, responsible for CO2 fixation, are annotated in all 16 strains (Table 4). Likewise, for all enzymes belonging to the pentose phosphate pathway (PPP), respective CLOGs are associated with all strains (Table 5). A more diverse picture is obtained for other key metabolic pathways. The enzyme FBP (fructose-1,6-bisphosphatase, EC 3.1.3.11) is not annotated for all strains and absent in all alpha-cyanobacteria, including the Prochlorococcus strains. However, taking into account results from a recent reconstruction and stoichiometric modeling of the strain Syn6803, the enzyme was found to be not essential for biomass formation [27]. To some extend, its function can also be substituted by the bifunctional enzyme SBP (fructose-1,6-/sedoheptulose-1,7-bisphosphatase, EC 3.1.3.37), present in all strains considered in this study. Likewise, the enzyme PFK (phosphofructokinase, EC 2.7.1.11) is not annotated for several strains, most notably again the Prochlorococcus strains. We note that PFK is essential for glycolysis, in its absence utilization of glycogen as a carbon and energy source has to proceed exclusively via the PPP. Other enzymes of the glycolytic pathway, such as FBA, GAP, PGM, and PYK are annotated for all strains (Table 4). In contrast, pyruvate metabolism, summarized in Table 5, is rather fragmented. While CLOGs annotated with the PEP carboxylase (PEPC, EC 4.1.1.31) are associated with all strains, the back reaction via the PEPKinase is rather rare and annotated only for three strains. PEPC catalyzes the anaplerotic conversion of PEP to oxaloacetate and inorganic phosphate Pi, and is essential for replenishment of TCA cycle intermediates. CLOGs annotated with the right-hand side of the TCA cycle, resulting in the formation of 2-oxoglutarate, are ubiquitous for all strains. The metabolite 2-oxoglutarate is considered to be a sensor for the nitrogen status of cyanobacteria [29] and serves as a precursor for several amino acids and nucleotides.


The diversity of cyanobacterial metabolism: genome analysis of multiple phototrophic microorganisms.

Beck C, Knoop H, Axmann IM, Steuer R - BMC Genomics (2012)

A pathway diagram of the cyanobacterial core metabolic network. Black boxes indicate enzymes whose corresponding CLOGs are associated with all 16 cyanobacterial strains. Grey boxes correspond to enzymes that are not annotated for one or more strains.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3369817&req=5

Figure 8: A pathway diagram of the cyanobacterial core metabolic network. Black boxes indicate enzymes whose corresponding CLOGs are associated with all 16 cyanobacterial strains. Grey boxes correspond to enzymes that are not annotated for one or more strains.
Mentions: Beyond storage compounds, Tables 4 and 5 summarize the presence of several key enzymes within cyanobacterial central metabolism across all 16 strains considered in this study. In contrast to Table 3, the tables do not distinguish between individual CLOGs associated with the same enzymatic function. A detailed depiction of individual CLOGs is provided as supplementary material (Additional File 6). For each enzyme usually a dominant CLOG exists in addition to a smaller number of secondary CLOGs. A graphical depiction of annotated pathways is given in Figure 8. Tables 4 and 5 allow for a detailed analysis of metabolic function. First, we note that all key enzymes of the Calvin-Benson cycle, responsible for CO2 fixation, are annotated in all 16 strains (Table 4). Likewise, for all enzymes belonging to the pentose phosphate pathway (PPP), respective CLOGs are associated with all strains (Table 5). A more diverse picture is obtained for other key metabolic pathways. The enzyme FBP (fructose-1,6-bisphosphatase, EC 3.1.3.11) is not annotated for all strains and absent in all alpha-cyanobacteria, including the Prochlorococcus strains. However, taking into account results from a recent reconstruction and stoichiometric modeling of the strain Syn6803, the enzyme was found to be not essential for biomass formation [27]. To some extend, its function can also be substituted by the bifunctional enzyme SBP (fructose-1,6-/sedoheptulose-1,7-bisphosphatase, EC 3.1.3.37), present in all strains considered in this study. Likewise, the enzyme PFK (phosphofructokinase, EC 2.7.1.11) is not annotated for several strains, most notably again the Prochlorococcus strains. We note that PFK is essential for glycolysis, in its absence utilization of glycogen as a carbon and energy source has to proceed exclusively via the PPP. Other enzymes of the glycolytic pathway, such as FBA, GAP, PGM, and PYK are annotated for all strains (Table 4). In contrast, pyruvate metabolism, summarized in Table 5, is rather fragmented. While CLOGs annotated with the PEP carboxylase (PEPC, EC 4.1.1.31) are associated with all strains, the back reaction via the PEPKinase is rather rare and annotated only for three strains. PEPC catalyzes the anaplerotic conversion of PEP to oxaloacetate and inorganic phosphate Pi, and is essential for replenishment of TCA cycle intermediates. CLOGs annotated with the right-hand side of the TCA cycle, resulting in the formation of 2-oxoglutarate, are ubiquitous for all strains. The metabolite 2-oxoglutarate is considered to be a sensor for the nitrogen status of cyanobacteria [29] and serves as a precursor for several amino acids and nucleotides.

Bottom Line: We describe genetic diversity found within cyanobacterial genomes, specifically with respect to metabolic functionality.Our results have direct implications for resource allocation and further sequencing projects.It can be extrapolated that the number of newly identified genes still significantly increases with increasing number of new sequenced genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute for Theoretical Biology, Humboldt-University of Berlin, Invalidenstr, 43, D-10115 Berlin, Germany.

ABSTRACT

Background: Cyanobacteria are among the most abundant organisms on Earth and represent one of the oldest and most widespread clades known in modern phylogenetics. As the only known prokaryotes capable of oxygenic photosynthesis, cyanobacteria are considered to be a promising resource for renewable fuels and natural products. Our efforts to harness the sun's energy using cyanobacteria would greatly benefit from an increased understanding of the genomic diversity across multiple cyanobacterial strains. In this respect, the advent of novel sequencing techniques and the availability of several cyanobacterial genomes offers new opportunities for understanding microbial diversity and metabolic organization and evolution in diverse environments.

Results: Here, we report a whole genome comparison of multiple phototrophic cyanobacteria. We describe genetic diversity found within cyanobacterial genomes, specifically with respect to metabolic functionality. Our results are based on pair-wise comparison of protein sequences and concomitant construction of clusters of likely ortholog genes. We differentiate between core, shared and unique genes and show that the majority of genes are associated with a single genome. In contrast, genes with metabolic function are strongly overrepresented within the core genome that is common to all considered strains. The analysis of metabolic diversity within core carbon metabolism reveals parts of the metabolic networks that are highly conserved, as well as highly fragmented pathways.

Conclusions: Our results have direct implications for resource allocation and further sequencing projects. It can be extrapolated that the number of newly identified genes still significantly increases with increasing number of new sequenced genomes. Furthermore, genome analysis of multiple phototrophic strains allows us to obtain a detailed picture of metabolic diversity that can serve as a starting point for biotechnological applications and automated metabolic reconstructions.

Show MeSH
Related in: MedlinePlus