Interactions of photosynthesis with genome size and function

Philosophical Transactions of the Royal Society B: Biological Sciences, Jul 2013

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

A PDF file should load here. If you do not see its contents the file may be temporarily unavailable at the journal website or you do not have a PDF plug-in installed and enabled in your browser.

Alternatively, you can download the file locally and open with any standalone PDF reader:

https://rstb.royalsocietypublishing.org/content/368/1622/20120264.full.pdf

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)


This is a preview of a remote PDF: https://rstb.royalsocietypublishing.org/content/368/1622/20120264.full.pdf

John A. Raven, John Beardall, Anthony W. D. Larkum, Patricia Sánchez-Baracaldo. Interactions of photosynthesis with genome size and function, Philosophical Transactions of the Royal Society B: Biological Sciences, 2013, 368/1622, DOI: 10.1098/rstb.2012.0264