Interactions of photosynthesis with genome size and function
Review
4
John A. Raven
1
3
4
John Beardall
2
4
Anthony W. D. Larkum
0
4
Patricia Sanchez-Baracaldo
4
5
6
0
Functional Plant Biology and Climate Change Cluster, University of Technology Sydney
,
New South Wales 2007
,
Australia
1
Present address: Division of Plant Science, University of Dundee at the James Hutton Institute, Invergowrie
,
Dundee DD2 5DA
,
UK
2
School of Biological Sciences, Monash University
,
Clayton, Victoria 3800
,
Australia
3
School of Plant Biology, University of Western Australia
,
35 Stirling Highway, Crawley, Western Australia 6009
,
Australia
4
One contribution of 14 to a Discussion Meeting Issue 'Energy transduction and genome function: an evolutionary synthesis'
5
School of Geographical Sciences, University of Bristol
,
Woodland Road, Bristol BS8 1SS
,
UK
6
School of Biological Sciences
Photolithotrophs are divided between those that use water as their electron donor (Cyanobacteria and the photosynthetic eukaryotes) and those that use a different electron donor (the anoxygenic photolithotrophs, all of them Bacteria). Photolithotrophs with the most reduced genomes have more genes than do the corresponding chemoorganotrophs, and the fastest-growing photolithotrophs have significantly lower specific growth rates than the fastest-growing chemoorganotrophs. Slower growth results from diversion of resources into the photosynthetic apparatus, which accounts for about half of the cell protein. There are inherent dangers in (especially oxygenic) photosynthesis, including the formation of reactive oxygen species (ROS) and blue light sensitivity of the water spitting apparatus. The extent to which photolithotrophs incur greater DNA damage and repair, and faster protein turnover with increased rRNA requirement, needs further investigation. A related source of environmental damage is ultraviolet B (UVB) radiation (280 - 320 nm), whose flux at the Earth's surface decreased as oxygen (and ozone) increased in the atmosphere. This oxygenation led to the requirements of defence against ROS, and decreasing availability to organisms of combined (non-dinitrogen) nitrogen and ferrous iron, and (indirectly) phosphorus, in the oxygenated biosphere. Differential codon usage in the genome and, especially, the proteome can lead to economies in the use of potentially growth-limiting elements & 2013 The Author(s) Published by the Royal Society. All rights reserved.
1. Introduction
The evolution of photosynthesis greatly increased the energy input to the
biosphere, supplementing energy from chemolithotrophy and from
photochemistry that is not catalysed by organisms, as well as from any less globally
significant energy sources [1]. Photosynthetic processes, including
energy-transducing rhodopsins as well as (bacterio)chlorophyll-based photochemistry, can
bring about some of the proton pumping, and hence adenosine triphosphate
(ATP) synthesis, in chemoorganotrophs, which would otherwise involve
oxidation of organic compounds. Here, the role of the photosynthetic reactions is
to decrease production of carbon dioxide from organic matter, while maintaining,
or increasing, the productivity of chemoorganotrophs [2,3]; the global upper limit
on these processes in the carbon cycle has been estimated [4]. The predominant
biogeochemical role of photosynthetic processes is, however, photolithotrophy:
that is, the autotrophic assimilation of carbon dioxide using some inorganic
reductant as the electron donor. Unless hydrogen is used as the electron donor,
photochemical energy input is needed to produce a reductant (often with
additional energy input from photogenerated ATP) capable of reducing carbon
dioxide to the redox level of carbohydrate. On Earth today, oxygenic
photolithotrophy assimilates carbon dioxide globally at over 100 Pg carbon per year in net
primary productivity; the corresponding numbers for anoxygenic
photolithotrophy and chemolithotrophy (mainly nitrification) are, respectively, 0.03 0.07 and
0.3 Pg C per year [5,6], although anoxygenic photolithotrophy
was quantitatively more important in the past [5 8].
However, photosynthetic organisms are not selected in
evolution for their contribution to global biogeochemistry:
the successful photosynthetic organisms leave more offspring
than their less successful competitors. The first question
considered in this paper is the extent to which photolithotrophy
means that organisms have a larger minimum number of
genes, larger minimum genome size, and a larger minimum
cell size, than organisms of similar cell organization but
living by chemoorganotrophy or chemolithotrophy.
A second area investigated is comparison of the maximum
specific growth rate among the three trophic modes in relation
to the extent of diversion of resources to catalysts and structures
related specifically to chemoorganotrophy, chemolithotrophy or
photolithotrophy. Consideration of the involvement in the
different trophic modes of highly expressed genes could help explain
any mismatch betw (...truncated)