Photosynthesis, arsenic and a window on the Archaean world

At the very base of the biological pyramid life is far simpler than that which we can see.  It takes the form of single cells that lack a nucleus and propagate only by cloning: the prokaryotes as opposed to eukaryote life such as ourselves. It is almost certain that the first viable life on Earth was prokaryotic, though which of its two fundamental divisions – Archaea or Bacteria – came first is still debated. At present, most prokaryotes metabolise other organisms’ waste or dead remains: they are heterotrophs (from the Greek for ‘other nutrition’). But there are others that are primary producers getting their nutrition by themselves, exploiting the inorganic world in a variety of ways: the autotrophs. Biogeochemical evidence from the earliest sedimentary rocks suggests that, in the Archaean prokaryotic autotrophs were dominant, mainly exploiting chemical reactions to gain energy necessary for building carbohydrates. Some reduced sulfate ions to those of sulphide, others combined hydrogen with carbon dioxide to generate methane as a by-product. Sunlight being an abundant energy resource in near-surface water, a whole range of prokaryotes exploit its potential through photosynthesis. Under reducing conditions some photosynthesisers convert sulfur to sulfuric acid , yet others combine photosynthesis with chemo-autotrophy. Dissolved material capable of donating electrons – i.e. reducing agents – are exploited in photosynthesis: hydrogen, ferrous iron (Fe2+), reduced sulfur, nitrite, or some organic molecules. Without one group, which uses photosynthesis to convert CO2 and water to carbohydrates and oxygen, eukaryotes would never have arisen, for they depend on free oxygen. A transformation 2400 Ma ago marked a point in Earth history when oxygen first entered the atmosphere and shallow water (see: Massive event in the Precambrian carbon cycle; January, 2012), known as Great Oxygenation Event (GOE). It has been shown that the most likely sources of that excess oxygen were extensive bacterial mats in shallow water made of photosynthesising blue-green bacteria that produced the distinctive carbonate structures known as stromatolites. These had formed in Archaean sedimentary basins for 1.9 billion years. It has been generally assumed that blue-green bacteria had formed them too, before the oxygen that they produced overcame the reducing conditions that had generally prevailed before the GOE. But that may not have been the case …

Microbial mats made by purple sulfur bacteria in highly toxic spring water flowing into a salt-lake in northern Chile. (credit: Visscher et al. 2020; Fig 1c)

Prokaryotes are a versatile group and new types keep turning up as researchers explore all kinds of strange and extreme environments, for instance: hot springs; groundwater from kilometres below the surface and highly toxic waters. A recent surprise arose from the study of anoxic springs laden with dissolved salts, sulfide ions and arsenic that feed parts of hypersaline lakes in northern Chile (Visscher, P.T. and 14 others 2020. Modern arsenotrophic microbial mats provide an analogue for life in the anoxic ArcheanCommunications Earth & Environment, v. 1, article 24; DOI: 10.1038/s43247-020-00025-2). This is a decidedly extreme environment for life, as we know it, made more challenging by its high altitude exposure to high UV radiation. The springs’ beds are covered with bright-purple microbial mats. Interestingly the water’s arsenic concentration varies from high in winter to low in summer, suggesting that some process removes it, along with sulfur, according to light levels: almost certainly the growth and dormancy of mat-forming bacteria. Arsenic is an electron donor capable of participating in photosynthesis that doesn’t produce oxygen. The microbial mats do produce no oxygen whatever – uniquely for the modern Earth – but they do form carbonate crusts that look like stromatolites. The mats contain purple sulfur bacteria (PSBs) that are anaerobic photosynthesisers, which use sulfur, hydrogen and Fe2+ as electron donors. The seasonal changes in arsenic concentration match similar shifts in sulfur, suggesting that arsenic is also being used by the PSBs. Indeed they can, as the aio gene, which encodes for such an eventuality, is present in the genome of PSBs.

Pieter Visscher and his multinational co-authors argue for prokaryotes similar to modern PSBs having played a role in creating the stromatolites found in Archaean sedimentary rocks. Oxygen-poor, the Archaean atmosphere would have contained no ozone so that high-energy UV would have bathed the Earth’s surface and its oceans to a considerable depth. Moreover, arsenic is today removed from most surface water by adsorption on iron hydroxides, a product of modern oxidising conditions (see: Arsenic hazard on a global scale; May 2020): it would have been more abundant before the GOE. So the Atacama springs may be an appropriate micro-analogue for Archaean conditions, a hypothesis that the authors address with reference to the geochemistry of sedimentary rocks in Western Australia deposited in a late-Archaean evaporating lake. Stromatolites in the Tumbiana Formation show, according to the authors, definite evidence for sulfur and arsenic cycling similar to that in that Atacama springs. They also suggest that photosynthesising blue-green bacteria (cyanobacteria) may not have viable under such Archaean conditions while microbes with similar metabolism to PSBs probably were. The eventual appearance and rise of oxygen once cyanobacteria did evolve, perhaps in the late-Archaean, left PSBs and most other anaerobic microbes, to which oxygen spells death, as a minority faction trapped in what are became ‘extreme’ environments when long before they ‘ruled the roost’. It raises the question, ‘What if cyanobacteria had not evolved?’. A trite answer would be, ‘I would not be writing this and nor would you be reading it!’. But it is a question that can be properly applied to the issue of alien life beyond Earth, perhaps on Mars. Currently, attempts are being made to detect oxygen in the atmospheres of exoplanets orbiting other stars, as a ‘sure sign’ that life evolved and thrived there too. That may be a fruitless venture, because life happily thrived during Earth’s Archaean Eon until its closing episodes without producing a whiff of oxygen.

See also: Living in an anoxic world: Microbes using arsenic are a link to early life. (Science Daily, 22 September 2020)

Salt and Earth’s atmosphere

It is widely known that glacial ice contains a record of Earth’s changing atmospheric composition in the form of bubbles trapped when the ice formed. That is fine for investigations going back about a million years, in particular those that deal with past climate change. Obviously going back to the composition of air tens or hundreds of million years ago cannot use such a handy, direct source of data, but has relied on a range of indirect proxies. These include the number of pores or stomata on fossil plant leaves for CO2, variations in sulfur isotopes for oxygen content and so on. Variation over time of the atmosphere’s content of oxygen has vexed geoscientists a great deal, partly because it has probably been tied to biological evolution: forming by some kind of oxygenic photosynthesis and being essential for the rise to dominance of eukaryotic animals such as ourselves. Its presence or absence also has had a large bearing on weathering and the associated dissolution or precipitation of a variety of elements, predominantly iron. Despite progressively more clever proxies to indicate the presence of oxygen, and intricate geochemical theory through which its former concentration can be modelled, the lack of an opportunity to calibrate any of the models has been a source of deep frustration and acrimony among researchers.

Yet as is often said, there are more ways of getting rid of cats than drowning them in butter. The search has been on for materials that trap air in much the same way as does ice, and one popular, if elusive target has been the bubbles in crystals of evaporite minerals. The trouble is that most halite deposits formed by precipitation of NaCl from highly concentrated brines in evaporating lakes or restricted marine inlets. As a result the bubbles contain liquids that do a grand job of preserving aqueous geochemistry but leave a lot of doubt as regards the provenance of gases trapped within them. For that to be a sample of air rather than gases once dissolved in trapped liquid, the salt needs to have crystallized above the water surface. That may be possible if salt forms from brines so dense that crystals are able to float, or perhaps where minerals such as gypsum form as soil moisture is drawn upwards by capillary action to form ‘desert roses’. A multinational team, led by Nigel Blamey of Brock University in Canada, has published results from Neoproterozoic halite whose chevron-like crystals suggest subaerial formation (Blamey, N.J.F. and 7 others, 2016. Paradigm shift in determining Neoproterozoic atmospheric oxygen. Geology, v. 44, p. 651-654). Multiple analyses of five halite samples from an ~815 Ma-old horizon in a drill core from the Neoproterozoic Canning Basin of Western Australia contained about 11% by volume of oxygen, compared with 25% from Cretaceous salt from China, 20% of late-Miocene age from Italy, and 19 to 22% from samples modern salt of the same type.

Salar de Atacama salt flat in the Chilean puna
Evaporite salts in the Salar de Atacama Chile (credit: Wikipedia)

Although the Neoproterozoic result is only about half that present in modern air, it contradicts results that stem from proxy approaches, which suggest a significant rise in atmospheric oxygenation from 2 to about 18% during the younger Cryogenian and Ediacaran Periods of the Neoproterozoic, when marine animal life made explosive developments at the time of repeated Snowball Earth events. Whether or not this approach can be extended back to the Great Oxygenation Event at around 2.3 Ga ago and before depends on finding evaporite minerals that fit stringent criteria for having formed at the surface: older deposits are known even from the Archaean.

Breathing spaces or toxic traps in the Archaean ocean


The relationship between Earth’s complement of free oxygen and life seems to have begun in the Archaean, but it presented a series of paradoxes: produced by photosynthetic organisms oxygen would have been toxic to most other Archaean life forms; its presence drew an important micronutrient, dissolved iron-2, from sea water by precipitation of iron-3 oxides; though produced in seawater there is no evidence until about 2.4 Ga for its presence in the air. It has long been thought that the paradoxes may have been resolved by oxygen being produced in isolated patches, or ‘oases’ on the Archaean sea floor, where early blue-green bacteria evolved and thrived.


A stratigraphic clue to the former presence of such oxygen factories is itself quite convoluted. The precipitation of calcium carbonates and therefore the presence of limestones in sedimentary sequences are suppressed by dissolved iron-2: the presence of Fe2+ ions would favour the removal of bicarbonate ions from seawater by formation of ferrous carbonate that is less soluble than calcium carbonate. Canadian and US geochemists studied one of the thickest Archaean limestone sequences, dated at around 2.8 Ga, in the wonderfully named Wabigoon Subprovince of the Canadian Shield which is full of stromatolites, bulbous laminated masses probably formed from bacterial biofilms in shallow water (Riding, R. et al. 2014. Identification of an Archean marine oxygen oasis. Precambrian Research, v. 251, p. 232-237).

English: Stromatolites in the Hoyt Limestone (...
Limestone formed from blue-green bacteria biofilms or stromatolites (credit: Wikipedia)

Limestones from the sequence that stable isotope analyses show to remain unaltered all have abnormally low cerium concentrations relative to the other rare-earth elements. Unaltered limestones from stromatolite-free, deep water limestones show no such negative Ce anomaly. Cerium is the only rare-earth element that has a possible 4+ valence state as well one with lower positive charge. So in the presence of oxygen cerium can form an insoluble oxide and thus be removed from solution. So cerium independently shows that the shallow water limestones formed in seawater that contained free oxygen. Nor was it an ephemeral condition, for the anomalies persist through half a kilometer of limestone.


The study shows that anomalous oxygenated patches existed on the Archaean sea floor, probably shallow-water basins or shelves isolated by the build up of stromatolite reef barriers. For most prokaryote cells they would have harboured toxic conditions, presenting them with severe chemical stress. Possibly these were the first places where oxygen defence measures evolved, that eventually led to more complex eukaryote cells that not only survive oxygen stress but thrive on its presence. That conjecture is unlikely to be fully proved, since the first undoubted fossils of eukaryote cells, known as acritarchs, occur in rocks that are more than 800 Ma years younger.