UV selective pressures and the development of an oxygenated

Ultraviolet (UV) Radiation (UVR), ∼400–100 nm, is the most energetic component of the solar spectrum which reaches the Earth, typically subdivided into the UV-A region (400–315 nm), the UV-B (315–280 nm) region, and the most energetic region, UV-C (280–100 nm). These high energy components can cause major disruptions to the bio- chemistry of life, often in the form of chemical bond breaking or free radical generation. Throughout the development of Earth’s atmosphere, the radiation which bombards the Earth’s surface has changed dramatically. Around 3 billion years ago in the Archean era of Earth’s history, when the earliest lifeforms on Earth are known to have existed, the atmosphere likely consisted predominately of: methane, ammonia, water vapour, carbon dioxide, nitrogen, hydrogen, hydrogen sulphide and various Noble gases, which together, at the theorised total surface pressure of 100 kPa are transparent to elec- tromagnetic radiation of wavelengths beyond _∼220 nm.121 _{Thus the solar spectrum}

reaching the Earth’s surface consisted of much UV-C radiation. As such, these early organisms were forced to migrate away from the surface, or develop other mechanisms in order to reduce exposure in order to survive.122

One such example is extant cyanobacterium, a phylum of bacteria, and one of the Earth’s earliest phototrophs, suggested to exist from at least ∼3 Giga-annum (Ga) ago.123 _{This organism has exhibited numerous mechanisms to strike a balance between}

obtaining sunlight for photosynthesis, whilst mitigating UV-C damage (Figure 2.7). (i) In the early ‘primordial soup’ water would have served as a UV-C attenuator, though several 10s of meters would be required for adequate protection, and thus would not be considered a surface habitat.121,124,128 _{(ii) Sedimentation in water certainly can atten-}

uate UV-C significantly, reducing the depth of water required. For example, inorganic salts such as sodium nitrate and sodium nitrite dissolved in water provide an attenuat- ing environment, and have been demonstrated to mitigate such damage for cyanobacte- ria,129 _{although the concentrations of such salts available during this period of Earth’s}

history are not well-known leaving this open to speculation. The presence of iron in such sediments has also been suggested as a likely candidate for early UV-C protection given only a small,_∼0.1%, of dopant in sediments would be required for significant UV-C at- tenuation.124,125 _{(iii) Fossil remains as well as present-day observations, for example at}

Surviving population Water (i) Sediments (ii) Matting (iii) Screening (iv) Excision (v)

Figure 2.7 | Suggested mechanisms of early photoprotection from UV-C radiation likely

utilised by cyanobacteria.124 (i) Tens of meters of water could provide protection for UV-C radiation,121 _{(ii) with the addition of sediments such as salts and iron, the depth required}

would be significantly reduced.124,125 (iii) Matting habitats are known to afford protection; the top layers (green hashes) are damaged or destroyed but provide protection to the lower lying population.126,127_{(iv) Screening molecules,e.g. pigmentation, have been identified which}

attenuate UV-C forming sheaths around a population.124 (v) In the event of UV-induced damage, to DNA for example, there exist enzyme controlled mechanisms which identify and repair damage, such as base excision (shown, oxidised guanine with adenine; a Hoogsteen base pair) and nucleotide excision.124

Here, upper layers reside in the path of UV-C radiation, blocking it for lower lying layers. Even in death, these upper layers of cells continue to provide photoprotection to those below until they lyse, and then need to be replaced.124,126,127 _{(iv) Organic screen-}

ing compounds, akin to present day skin pigmentation (discussed in Section 2.2.2), have been observed. Cyanobacteria can form protective sheaths with screening com- pounds such as scytonemin,131,132_{mycosporines,}132 _{flavonoids and carotenoids,}133 _{all of}

which can display strong absorption cross-sections in the UV-A and UV-B regions in present-day cyanobacteria, thus it is a tangible extrapolation that such pigmentation might have existed in the UV-C region during this period of Earth’s history.124 _(v)

In the event that UV-induced damage occurs, for example in Deoxyribonucleic Acid (DNA) where dimerisation or base-pair mismatch are known to occur via UV irra- diation (UV-A, UV-B and UV-C), sophisticated enzyme controlled identification and repair mechanisms, such as base-excision and nucleotide-excision, attempt to rectify the damage.132 _{It comes as no surprise that a number of these mechanisms were likely}

used together to strike a balance of meeting metabolic requirements, but reducing UV damage, to not only survive, but to thrive.

Moving forward in time, more complicated organisms and ecosystems such as large plant life on land masses, required a broad, efficient, and geographical photoprotection to thrive. This was, and still is, provided by today’s ozone rich stratosphere. Impor-

4

3

2

1

0

Age of Earth / Ga ago

100

10

1

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0.01

0.001

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tmospheric

O

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AL

Figure 2.8 |The development of an oxygen rich atmosphere happened after the GOEc. 2.45

Ga ago, the exact cause of which still remains elusive.138 _{Data reconstructed from Kump,}

figure 2.135

tantly however, it is only recently in Earth’s history that the oxygen content of the atmosphere could support such life, c. 500 Ma ago, let alone provide UV photoprotec- tion in the form of ozone (Figure 2.8). In the Archean era, oxygen levels were _∼10−5

of Present O2 Atmosphere Levels (PAL).134,135 There is evidence that oxygenic respira-

tion predates oxygenic photosynthesis, suggested from the phylogenetic reconstructions of cytochrome oxidase molecular sequences.136 _{This might be counter-intuitive but a}

reconciliation is found through the use of catalase enzymes which convert atmospheric hydrogen peroxide to water and oxygen.136 _{Despite this, the trace amounts of oxy-}

gen certainly point to early life being dominated by anoxygenic respiration, utilising sulphur-based energy sources like hydrogen sulphide, as well as oxidative-iron or UV mediated processes as electron donors for respiration.136_{Cyanobacteria are suggested to}

have evolved oxygenic photosynthesis,i.e. utilising oxygen as an electron donor as most life does today (a significantly more energy rich pathway), around 2.7 Ga ago.135–137

The summary of this is that atmospheric O2 levels remained essentially constant for

well over a Ga, before the Great Oxidation Event (GOE).

The GOE marks a ‘boom’ in atmospheric O2 levels, from ∼0.001 % PAL to ∼1 %

PAL in as little as 30 Ma, beginning some 2.45 Ga ago, see Figure 2.8.135 _{The exact}

cause of this event remain uncertain,138 _{but the time frame of this event has been well}

established through the measurement of 33_S/32_{S isotopic ratios in ancient rock forma-}

land masses likely formed,135 a new selective pressure towards oxygenic photosynthe- sis for cyanobacteria might have occurred,139,140 _{or perhaps geological changes in plate}

tectonics led to a decrease in oxygen demandvia subsequent oxygen reactions with vol- canic or metamorphic out-gassings.141,142 _{After the GOE, O}

2 levels varied minimally,

staying steady at _∼10 % PAL for over a Ga, sometimes dubbed the ‘boring billion’,143

where evolution appeared to stagnate, before another, smaller oxygen boom occurred marking the Cambrian era, during which an explosion in diversity of life and the de- velopment of complicated multicellular eukaryotic organisms persisted throughout the Phanerozoic era for another 500 Ma, and O2 atmospheric levels slowly reached 100%

PAL.144,145 _{After the GOE, atmospheric O}

2 levels would have been high enough for an

effective ozone layer, shielding subsequent organisms from harsh UV-C radiation, and thus the selective pressure of UV radiation is reduced, but not negligible given UV-A and UV-B radiation are only attenuated, rather than completely blocked by ozone.146

This has important consequences for present day organisms including both humans and plants, as is discussed in the next section.

2.2.2

Solar irradiation and its impact on the present day bio-