Cyanobacteria have developed an effective photosynthetic
CO2 concentrating mechanism (CCM) for improving the
efficiency of carboxylation by a relatively inefficient Rubisco. The
development of this CCM was presumably in response to the decline in
atmospheric CO2 levels and rising
O2, both of which were triggered by the development of
oxygenic photosynthesis by cyanobacteria themselves. In the past few years
there has been a rapid expansion in our understanding of the mechanism and
genes responsible for the CCM. In addition, there has been a recent expansion
in the availability of complete cyanobacterial genomes, thus increasing our
potential to examine questions regarding both the evolution and diversity of
components of the CCM across cyanobacteria. This paper considers various CCM
and photosynthesis gene components across eight cyanobacteria where
significant genomic information is available. Significant conclusions from our
analysis of the distribution of various genes indicated the following.
Firstly, cyanobacteria have developed with two types of carboxysomes, and this
is correlated with the form of Rubisco present. We have coined the terms
α-cyanobacteria to refer to cyanobacteria containing Form 1A Rubisco and
α-carboxysomes, and β-cyanobacteria having Form 1B Rubisco and
β-carboxysomes. Secondly, there are two NDH-1 CO2
uptake systems distributed variably,
withProchlorococcus marinus species appearing to lack
this CO2 uptake system. There are at least two
HCO3– transport systems
distributed variably, with some α-cyanobacteria having an absence of
systems identified in β-cyanobacteria. Finally, there are multiple forms
of carbonic anhydrases (CAs), but with only β-carboxysomal CA having a
clearly shown role at present. The α-cyanobacteria appear to lack a
clearly identifiable carboxysomal CA. A pathway for the evolution of
cyanobacterial CCMs is proposed. The acquisition of carboxysomes triggered by
the rapid decline of atmospheric CO2 in the Phanerozoic
is argued to be the initial step. This would then be followed by the
development of NDH-1 CO2-uptake systems, followed by the
development of low-and high-affinity
HCO3– transporters. An
intriguing question is, were carboxysomes developed first in cyanobacteria, or
did they originate by the lateral transfer of pre-existing proteobacterial
bacterial microcompartment genes? The potentially late evolution of the CCM
genes in cyanobacteria argues for a polyphyletic and separate evolution of
CCMs in cyanobacteria, algae, and higher plants.
Carbonic Anhydrases in Photosynthesizing Cells of C3 Higher Plants