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Interactions of photosynthesis with
genome size and function
John A. Raven1,†, John Beardall2, Anthony W. D. Larkum3
and Patricia Sánchez-Baracaldo4,5
rstb.royalsocietypublishing.org
Review
Cite this article: Raven JA, Beardall J, Larkum
AWD, Sánchez-Baracaldo P. 2013 Interactions of
photosynthesis with genome size and function.
Phil Trans R Soc B 368: 20120264.
http://dx.doi.org/10.1098/rstb.2012.0264
One contribution of 14 to a Discussion Meeting
Issue ‘Energy transduction and genome
function: an evolutionary synthesis’.
Subject Areas:
biophysics, cellular biology, ecology, evolution,
plant science
Keywords:
gene number, genome size, growth rate,
highly expressed proteins, oxygenic
photosynthesis, ultraviolet radiation
Author for correspondence:
John A. Raven
e-mail: [email protected]
†
Present address: Division of Plant Science,
University of Dundee at the James Hutton
Institute, Invergowrie, Dundee DD2 5DA, UK.
1
School of Plant Biology, University of Western Australia, 35 Stirling Highway, Crawley,
Western Australia 6009, Australia
2
School of Biological Sciences, Monash University, Clayton, Victoria 3800, Australia
3
Functional Plant Biology and Climate Change Cluster, University of Technology Sydney,
New South Wales 2007, Australia
4
School of Biological Sciences, and 5School of Geographical Sciences, University of Bristol,
Woodland Road, Bristol BS8 1SS, UK
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
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
& 2013 The Author(s) Published by the Royal Society. All rights reserved.
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Table 1 gives the number of genes and the number of kbp for a
number of genomes from free-living organisms, with an
emphasis on those with a small number of genes. While the
gene number is very important, the genome size is also
worth considering as an indicator of resource requirement to
replicate the genome, and, with gene number, the gene density.
The organisms with the smallest genomes (as reported in peerreviewed publications) found in free-living organisms occur in
the Archaea and Bacteria. Those photolithotrophic organisms
(oxygenic cyanobacteria) with the most reduced genomes
have more genes than do the chemoorganotrophs (Proteobacteria) with the most reduced genomes, but fewer genes than
the most reduced known genome of a chemolithotroph (autotrophic methanogenic Archaea) (table 1). This suggests that
relatively few specific genes are needed for osmochemoorganotrophy (¼ saprochemoorganotrophy): these genes involve
transport of solutes across the membrane and assimilation
into core metabolism. Table 1 suggests that a greater number
of specific genes are associated with autotrophy (chemolithotrophy and photolithotrophy); one category of such genes
involves those coding for autotrophic carbon dioxide assimilation. A further group of genes relate to the energy
transformation that converts the energy from reactions of inorganic compounds (in chemolithotrophy) or electromagnetic
radiation (in photolithotrophy). It should be emphasized that
these very small genomes are evolutionarily derived from
larger genomes, e.g. in Cyanobacteria [32].
Table 1 also shows the smallest reported genomes (in
peer-reviewed literature) for Eukarya of three trophic
2
Phil Trans R Soc B 368: 20120264
2. Gene number, genome size and cell size
modes. The number of protein-coding genes, and the
genome size in kbp, are smaller for fungal chemoorganotrophic osmotrophs than for the photolithotrophs; this is
the case for the corresponding trophic modes in Bacteria.
For Bacteria and Eukarya, the increment in gene numbers
for the photolithotrophs relative to chemoorganotrophic
osmotrophs is 178 and 613, respectively, while the increment
as a percentage is, respectively, 26% and 13%. It will be interesting to see how these values change when more genomes
are sequenced. There are no known genetically integrated
chemolithotrophic Eukarya, although the known metabolic
diversity of protists [33] means that this possibility cannot
be ruled out. The other entries for Eukarya in table 1 are
for chemoorganotrophic phagotrophs. The genome size and
number of genes coding for proteins are much greater for
the phagotrophic ciliate Tetrahymena thermophila than for
either of the other two trophic groups; the mechanistic basis
of this difference is not clear, although the volume of the ciliate
is a hundred times that of Schizosaccharomyces pombe and more
than a thousand times that of the photolithotrophic eukaryotes
in table 1. However, the other phagochemoorganotroph in
table 1, the choanoflagellate (opisthokont) Monosiga brevicollis,
has a volume similar to that of the osmochemoorganotroph
Schizosaccharomyces pombe, but it has more genes than the fission yeast (or the photolithotrophs) in table 1. To our
knowledge, there are no published values of gene number
and genome size for rather smaller phagochemoorganotrophs
such as the heterokont flagellate Cafeteria roenbergensis [34]. The
total gene number in any genome is likely to be greater than the
number of genes in the core genome for that trophic mode (i.e.
those genes found in all strains following a given trophic
mode); the estimate of the number of genes in the core
genome depends on how many organisms are examined and
how they are chosen. The core genome concept is central to
our understanding of the genomics of the Last Universal
Common Ancestor (LUCA) [35,36], with more general
discussion in [13–15,22–24,37–40].
It has been suggested that lateral gene transfer is limited
to accessory genes, but not core genes. However, this may
not be the case in the (photolithotrophic) cyanobacteria
Prochlorococcus and the marine strains of Synechococcus,
where core photosynthetic genes occur in cyanophages,
and in genomic islands [41,42]. Horizontal transfer of genes
coding for photochemical energy-transduction processes
can occur in plasmids in the mixotrophs (in the second
sense in the glossary), giving another means of horizontal
gene transfer [2,3]. Also associated with the photochemical
reactions of photosynthesis, is the case of the unicellular
cyanobacterium Acaryochloris marina, in which chlorophyll
d largely replaces chlorophyll a in photochemistry and
light-harvesting roles: this organism has a relatively large
genome with nine plasmids (but not as large as Nostoc) comprising 8528 protein-coding genes and with a size of 8362 kb
[19] (table 1). This has been interpreted in terms of an organism filling a relatively ‘uncompetitive’ niche, enriched in near
infrared radiation relative to 400–700 nm, where it is free to
diversify its metabolic strategies [19]. Support for this view
comes from the demonstration that A. marina has a much
higher rate of gene duplication than average cyanobacteria
and that certain gene duplications, in e.g. transcription,
carbohydrate transport and metabolism, ion transport
and metabolism and signal transduction, are positively
selected [43].
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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 between the small number of genes involved
specifically in a given trophic mode and the larger fraction of
cell protein involved specifically in that trophic mode. One
example of highly expressed genes is those for Rubisco, which
occurs in all oxygenic photolithotrophs and also in some anoxygenic phototrophs and in some chemolithotrophs [9–12].
Another set of highly expressed genes are those encoding the
apoproteins, which occur in all (bacterio)chlorophyll-based
photosynthetic systems. The third topic addressed is the
impact of the requirements for photosynthesis (exposure to
solar radiation) on photosynthetic organisms, and the effects of
local and global oxygenation on organisms directly as oxygen,
and indirectly through the availability of other resources.
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Table 1. Examples of the smallest reported genome size and gene number for free-living Bacteria, Archaea and Eukarya of a range of trophic modes from
peer-reviewed literature. For comparison, values are provided for a range of Cyanobacteria.
chemoorganotrophic bacteria
SAR11 (e.g. Pelagibacter ubique)
number of protein-coding genes
genome size (kbp)
references
1237– 1457
[13,14]
b-Proteobacterium HTCC2181
oxygenic photolithotrophic cyanobacteria
1338
1304
[15]
Prochlorococcus marinus
1716 – 3022
1643– 2683
[16]
Raphidiopsis brookii
Cylindrospermopsis raciborskii
3968
3088
3890
3200
[17]
[17]
Nostoc punctiforme
Acaryochloris marina
6501
8528
8941
8362
[17,18]
[19]
12 356
12 073
[20]
Chlorobium tepidum TLS
2288
2154
[21]
chemolithotrophic methanogenic archaeans
Methanocorpusculum labreanum
1828
1805
[22,23]
Methanobacterium thermoautotophicum
chemoorganotrophic osmotrophic eukaryotes
1855
1751
[24]
Ashbya gosypii
4718
9200
[25]
Schizosaccharomyces pombe
chemoorganotrophic phagotrophic eukaryotes
4824
13 800
[26]
9196
27 000
41 600
104 000
[27]
[28]
photolithotrophic eukaryotes
Cyanidioschyzon merolae
5331
16 520
[29]
Ostreococcus lucimarinus
7651
13 200
[30]
Ostreococcus tauri
7892
12 699
[30,31]
Scytonema hofmanii
anoxygenic photolithotrophic bacterium
Monosiga brevicollis
Tetrahymena thermophila
Having a low gene number and dense gene packing permits
cells to be very small (0.5 mm equivalent spherical diameter),
without the genome taking up a greater fraction of the cell
volume than is the case for larger cells with larger genomes.
This relates to ‘scalability’ [44,45]. Genome reduction in Pelagibacter [46] and Prochlorococcus [32,47] may be related to specialization
to oligotrophic habitats [16,47,48]. In contrast, larger genomes in
some cyanobacteria were found in lineages from more variable
habitats, e.g. microbial mats or inter-tidal zones (table 1)
[20,32]; these habitats are often associated with more complex
morphologies such as filamentous and multicellular forms [49].
Recent analyses have shown that the morphologically complex
true-branching cyanobacterium Scytonema hofmanni PCC 7110
is the most gene-rich prokaryote currently known, with 12356
protein-coding genes in its 12073 kbp genome [20]. Phylogenetic
and genomic studies have shown a clear trend in the reduction
of genome size in the evolution of Prochlorococcus [50,51],
which dominate in habitats of low nutrient availability. Those
Prochlorococcus genotypes growing near the thermocline/pycnocline are exposed to higher nutrient concentrations, but intercept
lower fluxes of photosynthetically active radiation [47].
Reduction in genome size has not only been observed
within planktonic cyanobacteria (e.g. Prochlorococcus) but also
in some symbiotic cyanobacteria [32] in which a reduced
genome size might be indicative of their life style. The
smallest genome (1400 kbp) found so far is the one from
cyanobacterium U-CYNA [52], which is symbiotic with a
small-celled prymnesiophycean alga [53]. Cyanobacterium UCYNA lacks essential components of the photosynthetic
machinery (e.g. 127 orthologues present in all other cyanobacterial genomes), including photosystem II, carboxysomes (i.e.
the cyanobacterial microcompartments where CO2 fixation
takes place using Rubisco as the terminus of the CO2 concentrating mechanism) and enzymes specific to the Calvin–
Benson cycle, so that it cannot carry out autotrophic CO2
fixation or O2 production from water [54]. Less severe
genome reductions have been identified in other obligate symbionts such as Nostoc azollae 0708 [32]. Turning to more obvious
cases of obligate symbiosis, but one not involving diazotrophy,
the chromatophore of the euglyphid (rhizarian) amoeba
Paulinella chromatophora is an a-cyanobacterium (similar to
Prochlorococcus and open ocean Synechococcus) coding for all
photosynthetic components but lacking many enzymes
involved in amino acid synthesis, and so depends on the
amoeba for these amino acids [55,56]. The chromatophore
genome has 867 protein-coding genes and is 1021 kbp in size
[55]. There are also apparently genetically integrated diazotrophic cyanobacteria in some freshwater diatoms, such as
Epithemia and Rhopalodia [57–59]. The extent of genome
reduction in this case is not known, but the estimated genome
Phil Trans R Soc B 368: 20120264
1357 – 1541
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trophic mode, organism
3
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Table 2. Specific growth rates of Bacteria and Archaea of a range of
trophic modes. From [80 – 84]. Rates normalized to 20 8C assuming a Q10
of 2. Rates are the maximum values for the trophic mode, with the
exception of a very small-celled osmochemoorganotroph from the SAR11
clade of a-proteobacteria [84] and the very small-celled photolithotrophic
cyanobacterium Prochlorococcus [83,85]. The units of specific growth rate
are increment of cell numbers per cell per second.
organism and trophic mode
283
aerobic osmochemoorganotroph SAR11 clade
(e.g. Pelagibacter ubique)
10
aerobic chemolithotroph
48
Alcaligenes eutrophus
anaerobic chemolithotroph
15
Methanococcus vannielii
anoxygenic photolithotroph
27
Chlorobium limicola
oxygenic photolithotroph Synechococcus sp.
24
oxygenic photolithotroph Prochlorococcus
7
CCMP 1378
Microalgae (including Cyanobacteria) often show a less
clear relationship between specific growth rate and RNA
content than do many other organisms [70]. The smallest
microalgae (including Cyanobacteria) have lower maximum
specific growth rates than cells with 3–10 times the equivalent cell diameter, and larger genomes [71 –78]. These
data for Cyanobacteria and microalgae do not therefore
lend support to the concept of maximizing growth rate by
minimizing genome size.
A final point concerns the number of genes, and size in kbp,
of the genomes of Archaea and Bacteria relative to the nuclear
genome of Eukarya (table 1) [79]. There is clearly an overlap in
the size of the cyanobacterial genomes and those of photolithotrophic Eukarya (table 1). Evidently, the very small cells
of the smallest eukaryotic photolithotrophs do not make use
of the potential for a larger number of genes permitted, on
energetic grounds, by the eukaryotic condition [78].
3. Highly expressed genes and maximum specific
growth rate
There are clear differences in specific growth rates (adjusted
to 20 8C, assuming a Q10 of 2) between the fastest-growing
chemoorganotrophic microbes and those of autotrophic
microbes of a similar cell size (tables 2 and 3). Table 2 shows
data for osmochemoorganotrophic Bacteria, chemolithotrophic
Archaea and Bacteria, anoxygenic photolithotrophic bacteria
and the oxygenic photolithotrophic cyanobacteria. Table 3
shows data for Eukarya, including osmochemoorganotrophic and phagochemoorganotrophic, photolithotrophic and
also mixotrophic (combining phototrophy with osmotrophy
and phagotrophy).
Phil Trans R Soc B 368: 20120264
aerobic osmochemoorganotroph
Escherichia coli
specific growth
rate (3 106 s21)
4
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size is 2600 kbp, which is less than that of free-living diazotrophic cyanobacteria but more than that of the smallest genome
(table 1) in non-diazotrophc free-living cyanobacteria [57].
Some of the consequences of genome reduction involving
significant decreases in metabolic capabilities are indicated
by the following three examples, two from oxygenic photolithotrophs and one from osmochemoorganotrophs. (i) Many
Prochlorococcus genotypes cannot use NO2
3 as a N-source and
some cannot use NO2
2 : these genotypes need less energy for
growth on reduced N, but do not have the option of using
the more energy-expensive N source when it is available [60].
(ii) Prochlorococcus has no catalase, and so cannot dispose of
photosynthetically produced H2O2 without ‘helper’ chemoorganotrophic bacteria [61,62]. (iii) The a-proteobacterial clade
SAR11 (e.g. Pelagibacter ubique) can only use reduced S sources
such as methionine and dimethylsulfoniopropionate; other
marine saprochemoorganotrophic a-proteobacteria can use
SO22
4 [46]. The use of reduced S sources needs less energy for
growth, but SAR-11 does not have the option of using the
more energy-expensive SO22
4 , which is much more abundant
in the sea and many other aquatic and terrestrial habitats [46].
It must, however, be pointed out that loss of genes, and hence
loss of the associated function, is not restricted to minimal
genomes. An example from the eukaryotic algae is the loss of
the vitamin B12-independent pathway of methionine synthesis
involving MetH, leaving the vitamin B12-dependent pathway
involving MetE [63,64]. Since eukaryotes are unable to synthesize
vitamin B12, the loss of MetH means that the growth of the cells in
the absence (as is usually the case in nature) of external methionine depends on the provision of vitamin B12 from the organisms
which can synthesize it, i.e. Archaea and Bacteria. This provision
can either occur through the aqueous environment or by a symbiotic relationship of the producer organism and eukaryotic
algae [63]. Of the 306 algal species from a range of clades examined, more than half needed vitamin B12 [63]. Estimates of the
times at which MetH was lost in the chlorophycean order Volvocales shows that this process of gene loss is continuing [64].
Minimization of nuclear genome size does not seem to be a
rationale for gene loss in the Volvocales, since there are an
order of magnitude more protein-coding genes (14 516–14 520)
and two orders of magnitude more base pairs (118–158 Mbp)
in the nuclear genome of the Volvocales [65] than in Prochlorocococcus (table 1). For comparison, the smallest known nuclear
genome in green algae, that of the prasinophycean Ostreococcus,
has 8166 protein-coding genes densely packed in a 12.56 Mbp
genome in O. tauri, according to Develle et al. [31], while
Palenik et al. [30] quote 7892 and 7651 protein-coding genes
and 12.6 and 13.2 Mbp for O. tauri and O. lucimarinus, respectively. Palenik et al. [30] point out that Ostreococcus lacks MetH
and so requires vitamin B12. In this instance, with the smallest
nuclear gene number known for green algae, it is possible
to argue that loss of MetH might, in this case, be related to
genome minimization.
Despite the small (1.66 Mbp) genome size, over half of
cellular P in P-limited Prochlorococcus MED4 is in DNA [66].
It has been suggested [66] that there is a role of P (and N)
limitation in selecting for small genomes in organisms in Plimited environments and that this leaves more P available
for RNA, allowing more rapid growth; however, this may
not be universally applicable [67–69]. Also, there is often a
negative correlation between maximum specific growth rate
and genome size, and a positive correlation between specific
growth rate and RNA content [67,69].
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organism and trophic mode
Osmochemoorganotroph Achlya bisexualis
(oomycete)
specific growth
rate (3 106 s21)
170
88
Chemophagotroph Paraphysomonas
69
imperforata (Chrysophyceae)
Photophagotroph Ochromonas sp.
32
(Chrysophyceae)
Photolithotroph Dinobryon divergens
12
(Chrysophyceae)
(D. divergens usually grows
photophagotrophically)
Photoosmotroph Chlorella regularis
(Trebouxiophyceae)
40
Photolithotroph Chlorella regularis
(Trebouxiophyceae)
27
Photolithotroph Chaetoceros salsugineum
75
(Bacillariophyceae)
The fastest-growing chemoorganotrophs have significantly
higher specific growth rates than the fastest-growing photolithotrophs in both Bacteria and Eukarya. This slower growth
of photosynthetic organisms apparently results from diversion
of resources into the photosynthetic apparatus that can account
for up to half of the cell protein (table 4). A further diversion of
protein, and of RNA, in that fraction of the cellular ribosomal
complement (a fraction of the cytosolic ribosomes, and all of
the ribosomes in the plastids) are related to the synthesis
of the photosynthesis-specific proteins. In eukaryotic algae,
the plastids occupy up to half of the ‘metabolic’ cell volume,
i.e. excluding vacuoles, storage granules and cell walls and
other extracellular structures (table 5). The situation regarding
protein allocation to chemolithotrophy-specific components
of the methanogenic Archaea in table 2 is less clear. Less
effort seems to have been made to determine the allocation of
proteins (and RNA) to synthesizing and maintaining the
chemolithotrophy-specific components of the cell machinery
than is the case for photolithotrophy-specific components.
4. Photosynthesis-related damage to nucleic
acids and proteins
All electron transfer reactions in the presence of molecular
oxygen carry the danger of producing reactive oxygen species
(ROS), with their damaging effects on cell constituents [94,95].
Oxygenic photosynthesis is especially susceptible to this
problem because the redox level needed to drain electrons
from water (greater than þ0.8 V) by the reaction centre of
5
Phil Trans R Soc B 368: 20120264
Phagochemoorganotroph Tetrahymena geleii
(ciliate)
photosystem II leads to the generation of much singlet
oxygen; the fact that the major protein involved, D1, is the fastest turning-over protein known is a testament to the
unavoidable damage incurred by the water splitting mechanism [96]. We will discuss the extent to which other protective
measures fail and involve greater DNA damage and repair,
and faster protein turnover than in chemoorganotrophs, with
implications for energetics and rRNA expression. We will
also comment on possible implications for the location of
genes within the eukaryotic cell. A related source of environmental damage is UVB radiation, the flux of which decreased
at the Earth’s surface as oxygen (and ozone) increased in the
atmosphere; possible relict UV avoidance and repair mechanisms from the times of higher UV fluxes will be discussed.
Local, and then global, oxygenation in the Great Oxygenation
Event (GOE) some 2.32 Ga [97] led to the much-discussed
requirements of defence against ROS and the opportunity for
aerobic respiration for organisms in the oxygenated habitats.
However, there are also effects on the nitrogen, phosphorus
and iron cycles that decrease the availability to organisms of combined (non-dinitrogen) nitrogen, phosphorus and ferrous iron in
the oxygenated biosphere. The effects on combined nitrogen and
ferrous iron are relatively direct and occurred at, or soon after, the
GOE [98]. The decreased availability of phosphorus was delayed,
and related to the decrease in silicic acid concentration in the surface ocean, which decreases the competition between silicic acid
and phosphate in the scavenging of phosphate by iron [99]. The
removal of silicic acid depended on the evolution of silicified
eukaryotes about 550 Ma (radiolarians, sponges) and, especially,
diatoms approximately 120 Ma. There are implications of the
decreased availabilities of these nutrient elements for the evolution of novel pathways related to enhancing the availability
of these elements and/or decreasing the requirement for
them. There is also the possibility of an influence of photosynthesis on variations in codon usage, which could economize in
the use of potentially growth-limiting elements in the genome
and, especially, the proteome, but this is not discussed in detail
here [12,100,101].
The GOE involved O2 production by oxygenic photosynthesis, which evolved in Cyanobacteria [102]. Evolution of the
water splitting apparatus, involving a manganese– calcium
complex, exposed all organisms that use this apparatus to
two vulnerabilities: (i) production of singlet oxygen, noted
above, and (ii) blue light and UVB inhibition [103–105].
Recent work, combining phylogenomic and character evolution analyses, has shown that Cyanobacteria originated in
freshwater environments [20,49,102]. The small area of freshwaters means that the global biogeochemical impact of
oxygenic photosynthesis was minimal until Cyanobacteria
started colonizing the marine environment (approx. 2.32 Ga),
which currently covers more than two-thirds of the Earth’s surface [102]. Furthermore, marine cyanobacteria do not form a
natural group or monophyletic clade, but they are clustered
with freshwater species within the cyanobacterial radiation,
providing further evidence for independent colonization
events into marine environments [49,102]. As well as the possibility of respiration with O2 as the terminal electron acceptor,
the GOE also increased the possibility of damage to cells by
ROS. Decreased ROS production from the interaction of UV
radiation with (even anoxic) water [106], as a result of
decreased UV flux at the Earth’s surface as atmospheric
oxygenation led to increasing stratospheric O3, is outweighed
by ROS production from intracellular O2 [94]. A specific
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Table 3. Maximum specific growth rates of microscopic Eukarya of a range
of trophic modes; all aerobic. From [80 – 82]. Rates normalized to 20 8C
assuming a Q10 of 2. Units of specific growth rate are increment of cell
numbers per cell per second.
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Table 4. Fraction of cell protein content of Cyanobacteria and microscopic eukaryotic algae occupied by the highly expressed photosynthetic proteins Rubisco
and apoproteins of reaction centre and light-harvesting complexes, and for comparison the ribosomal proteins.
references
comments
Rubisco
0.03– 0.16
[86]
most data from algae expressing CCMs grown at high light. Some values assume a conversion
0.02– 0.06
[87]
factor for chlorophyll to cell protein
values all based on direct estimates of Rubisco protein and total protein
[9,11]
a saving of about a third of the protein requirement for a given rate of carbon dioxide fixation
apoproteins of pigment– protein complexes
0.04– 0.4
[88 – 90]
ribosomal proteins
0.09– 0.21
highest values for algae growing at low light)
[90]
Table 5. Fraction of ‘metabolic volume’ (cell volume minus walls and
vacuoles) occupied by chloroplasts in microalgae (mainly freshwater) grown
photolithotrophically [89,91 –93]. n ¼ number of species examined.
Chlorophyta
0.33– 0.61 (n ¼ 3)
Euglenophyta
Cryptophyta
0.15– 0.5 (n ¼ 2)
0.69 (n ¼ 1)
Haptophyta
0.34– 0.40 (n ¼ 2)
Bacillariophyceae
Dinophyta
0.39– 0.56 (n ¼ 6)
0.07– 0.32 (n ¼ 2)
damaging effect of O2 is the irreversible damage to nitrogenase
[101,107,108], and through singlet oxygen formation, O2 also
contributes to photodamage to the D1 protein of photosystem
II, resulting in photoinhibition [96,107,109]. In addition to the
energy cost [110] of synthesis of replacement nitrogenase and
photosystem II components (mainly D1 protein, the psbA
gene product), Raven [101] argues that there is also a significant
diversion of rRNA from other significant protein syntheses, at
least under P limitation and with optimal allocation of
resources, and also the occurrence of additional genes related
to protection and repair [101,109]. Competition of O2 with
CO2 at the active site of Rubisco, which evolved in anoxic
conditions, does not involve damage by O2 [12,107,111].
Despite these energetic and other constraints, some photosynthetic organisms can grow rapidly at up to four times airequilibrium O2 concentration, e.g. in high intertidal rock
pools and stromatolites, and in bundle sheath cells of terrestrial NADme and PEPck C4 flowering plants [112], and nonphotosynthetic organisms occur in the rock pools and as endobionts in stromatolites. It would be predicted that there would
be more oxygen-related protein damage, hence more protein
resynthesis, in oxygenic photosynthetic cells than in nonphotosynthetic aerobic cells, as a result of the production of
singlet oxygen in photosynthesis, noted above. Moreover, at
least in the light, the O2 concentration in oxygenic photosynthetic cells is higher that it is in the medium, while for nonphotosynthetic cells the intracellular O2 concentration in the
respiring cells is less than that in the medium. It would also
be predicted that there would be more protein damage, and
hence more protein re-synthesis, in aerobic cells than in
anaerobic cells. However, there seem to be no appropriate
good comparative data that test these predictions [110].
The green sulfur bacterium Chlorobium tepidum can only grow
photolithotrophically in the absence of oxygen and grows at, or
just below, the oxycline in water bodies [21]. Although this organism is normally exposed to low fluxes of the wavelengths that it
can use in photosynthesis (400–840 nm) and correspondingly
low fluxes of UVB, and is generally not exposed to O2, the complete genome sequence shows that the organism has a large suite
of genes coding for proteins involved in DNA repair, as well as
genes coding for enzymes that scavenge ROS and so might
help them to protect various oxygen-damaged enzymes in
photosynthesis and nitrogenase [21]. The presence of superoxide
dismutase is typical of aerotolerant anaerobes and aerobes, but
not generally of obligate anaerobes [113,114]. It is likely that at
least some of these DNA repair and free radical scavenging
enzymes are expressed in the absence of an increased threat of
damage as a precautionary step, and that at least the free radical
scavenging enzymes were absent before the GOE.
Turning to damage by UVB, organisms that intercept
photosynthetically active radiation (PAR) (including, to a
varying extent, ultraviolet A (UVA) radiation) also intercept
some damaging ultraviolet radiation (UVR) (UVB þ UVA).
UVR is attenuated more than PAR by water and the substances dissolved in it [111,115]. UVA (320– 400 nm) is
damaging to some oxygenic photosynthetic organisms [116]
but may be used by others in metabolic and developmental
regulation. Regulation related to absorption of UVA involves
the long wavelength tail of UVB pigments such as UVR8
[117] and the short wavelength tail of the blue light-UVA pigments cryptochrome and phototropin [118], as well as via a
specific but poorly characterized photoreceptor [119]. Furthermore, UVA can be a significant source of energy for
some anaerobic photosynthetic bacteria (on the basis of
bacteriochlorophyll absorption spectra) [120] and algae
[121–125]. UVB (280–320 nm) screening and damage repair
are required by both anoxygenic [21] and oxygenic phototrophs, with the need for additional genes (see above).
Organisms at other trophic levels in habitats in which they
intercept solar radiation, e.g. in grazing on, or parasitizing,
photolithotrophs, also need UVB protection and repair mechanisms. Small cells have smaller package effect, so (other
things being equal) are less readily protected by ultraviolet
Phil Trans R Soc B 368: 20120264
could be achieved by replacing the Rubisco Benson– Calvin cycle with one of the alternative
autotrophic carbon dioxide fixation pathways
rstb.royalsocietypublishing.org
fractionation of cell protein
6
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5. Conclusions
More genes may be needed to support the core processes
of autotrophy (chemolithotrophy, photolithotrophy) than for
osmochemoorganotrophy, if not for phagoorganotrophy.
This agrees with the finding that, on the basis of peer-reviewed
data, autotrophs have larger minimal genome sizes than
chemoorganotrophs.
Small genome and cell size do not always mean faster growth
rate and more rapid energy conversion; the smallest archaeal and
bacterial cells with a given trophic mode grow less rapidly than
cells with cell volumes 1–2 orders of magnitude greater. The
diversion of a large proportion of resources into the photosynthetic apparatus means that phototrophic organisms tend to
exhibit slower growth rates than chemoorganotrophs.
Changes in the global environment with implications for
cellular energetics, such as the GOE, might be related to
changes in codon usage, leading in turn to economies in C
and S usage but not in N. Variations in GC:AT are not generally related to high UVB fluxes in the natural environment.
UVB fluxes incident on organisms would have been greater
before the GOE, and the GC:AT effect may have been greater
before the evolution of oxygenic photosynthesis and the
subsequent GOE
J.A.R. thanks John Allen, Jason Bragg, Paul Falkowski, Zoe Finkel,
Kevin Flynn, Mario Giordano, Andrew Knoll, Hans Lambers, Enid
MacRobbie and Antonietta Quigg for their contributions. The University of Dundee is a registered Scottish charity, No. SC015096.
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Glossary
autotroph
chemolithotroph
chemoorganotroph
an organism using exergonic
inorganic chemical reactions, or
photons, as the energy source for
growth and inorganic chemicals
taken up on a molecule-by-molecule
basis across the plasmalemma to
supply nutrient elements.
an organism using the catalysis of
exergonic inorganic chemical reactions as the energy source for
growth and inorganic chemicals
taken up on a molecule-by-molecule
basis across the plasmalemma to
supply nutrient elements.
an organism using the catabolism
of organic compounds as the
energy source for growth, and
genetically integrated
heterotroph
osmochemoorganotroph
organic compounds as the source
of carbon and, in many cases,
the source of nitrogen.
used of endosymbionts: an endosymbiont that has transferred
some genes needed for independent growth to the host nuclear
genome, with loss of these genes
from the endosymbiont genome.
Vertically transmitted.
chemoorganotroph
a chemoorganotrophic organism
taking up organic and inorganic
nutrients on a molecule-by-molecule
basis
across
the
plasmalemma as the means of
acquiring carbon and other
elements.
10
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mixotroph
11
Phil Trans R Soc B 368: 20120264
phagochemoorganotroph a chemoorganotrophic organism
taking up particles of live or
dead organic matter as their
means of acquiring carbon and
other elements.
photolithotroph
an organism using photons as the
energy source for growth and
inorganic chemicals taken up on
a molecule-by-molecule basis
across the plasmalemma to
supply nutrient elements.
saprochemoorganotroph osmochemoorganotroph.
rstb.royalsocietypublishing.org
(i) an organism combining autotrophy
and
chemorganotrophy;
usually applied to phototrophic
autotrophs. (ii) An osmochemoorganotroph that has no mechanism
of autotrophic carbon dioxide fixation,
but
which
has
a
photochemical apparatus that generates ion gradients and ATP that
can supplement and partially
replace the generation of ion gradients and ATP by catabolism of
organic compounds.