How microbes learned to build rock, and kept building it for three and a half billion years. A story told in layers, from the first shallow seas to the few lagoons and lakes where it still happens today.
The oldest widely accepted traces of life on Earth are layers: thin sheets of sediment that microbes trapped, bound and hardened into rock.
In the Pilbara of Western Australia, the Dresser Formation holds stromatolites, palisade-like microbial fabrics and gas bubbles preserved in what appears to be mineralised slime, all laid down around hot springs about 3.48 billion years ago. They push the record of inhabited hot springs on land back by about three billion years (Djokic et al. 2017). Nearby, the 3.43 billion-year-old Strelley Pool Formation preserves a whole stromatolite reef (Allwood et al. 2006).
Rocks built this way are called microbialites, a word coined in 1987 for sediments formed by communities of microbes living on the bottom of lakes, lagoons and seas (Burne and Moore 1987). Stromatolites are the layered kind.
In living stromatolites, filamentous cyanobacteria glide up through settling sand and glue the grains in place with sticky extracellular polymers.
Microbial metabolism shifts the water chemistry inside a mat until calcium carbonate crystallises, a balance Visscher and colleagues call the alkalinity engine (Dupraz et al. 2009).
Cone-shaped structures in 3.7 billion-year-old rocks from Isua, Greenland were proposed as stromatolites in 2016, then reinterpreted as deformation features (Allwood et al. 2018). Shape alone does not prove life.
Hot-spring stromatolites like the Pilbara’s offer an analogue for where to look for signs of life in ancient hot springs on Mars (Djokic et al. 2017).
The microbes building these layers changed the planet. Cyanobacteria, many of them living in mats and stromatolites, had evolved a way to split water with sunlight, releasing oxygen.
Around 2.4 billion years ago that oxygen began to build up in the atmosphere. The Great Oxidation Event permanently changed Earth’s chemistry and opened the way for complex life.
Mats did more than make oxygen. With high metabolic rates and tightly coupled element cycles, they shifted the oxidation state of Earth’s surface through both oxygen and hydrogen production (Dupraz et al. 2009).
In a living mat, photosynthesis pushes oxygen above saturation by day. At night it vanishes from all but the top fraction of a millimetre and sulfide rises toward the surface. Watch it happen.
Photosynthesis that uses sulfide or iron instead of water is older. Visscher and colleagues study permanently oxygen-free, arsenic-based mats in Chile’s Atacama as an analogue for that world (Visscher et al. 2020).
For nearly two billion years, through the Proterozoic eon, stromatolites were the reefs of the world.
Between 2.5 billion and 541 million years ago, stromatolites reached their greatest abundance and variety, building domes, columns, branching thickets and cones in shallow seas. Cut one open and its interior usually falls into one of four fabrics.
Laminated, with layers stacked like pages.
Clotted clumps. Pavilion Lake and Lake Clifton build these.
Branching, like shrubs.
No clear internal structure.
Then stromatolites became rare.
As animals diversified in the Cambrian, about 540 million years ago, stromatolites declined sharply. Grazing and burrowing animals and competition from algae are the leading explanations, though the causes are still debated.
Today living microbialites persist mostly where animals and algae struggle: water that is unusually salty, cold, nutrient-poor or chemically extreme.
Hamelin Pool in Shark Bay is about twice as salty as the open ocean.
Pavilion Lake in British Columbia is cold and nutrient-poor.
In the Bahamas, stromatolites grow in ordinary seawater.
Stromatolites were first named from fossils, in 1908. Then geologists found them growing.
The living stromatolites of Hamelin Pool in Shark Bay are described in the scientific literature, giving geologists a modern analogue for the fossil record (Logan 1961).
Stromatolites growing in open water at normal marine salinity are found in the Bahamas, first at the Schooner Cays (reviewed in Visscher et al. 1998).
Robert Burne and Linda Moore coin the word microbialite for all sediments built by bottom-dwelling microbial communities.
Shark Bay is inscribed as a World Heritage Area. Hamelin Pool is recognised as the one place where living stromatolites show a range of forms comparable to the fossil record (DBCA).
Molecular surveys reveal unexpected bacterial and archaeal diversity inside Shark Bay stromatolites (Burns et al. 2004).
At Highborne Cay in the Bahamas, Pamela Reid, Pieter Visscher and colleagues worked out how a living stromatolite builds its layers. Step through one cycle, and keep going to grow your own column.
Sand arrives. Pioneer communities of gliding filamentous cyanobacteria move up through the settling grains and bind them in place.
Sedimentation pauses. A film of extracellular polymers spreads over the surface. Heterotrophic bacteria, sulfate reducers among them, break it down, and a thin crust of microcrystalline carbonate forms.
During a long pause a mature community develops, including coccoid cyanobacteria that bore into the grains. They weld the surface into a thicker, well-lithified lamina.
Step 1 of 3Layers added: 0
Based on Reid, Visscher et al. 2000 and Visscher, Reid and Bebout 2000.
Metagenomics reads the DNA of a whole community at once. Turned on microbialites by the White, Burns and Visscher groups, it rewrote the cast list.
Pavilion Lake microbialites differ from the surrounding sediment and water, are enriched in cyanobacteria and acidobacteria, and carry abundant antiviral genes (White et al. 2016). Microbialites in a flooded asbestos mine at Clinton Creek turned out to be functionally similar to polar mats, and richer than the sediment in genes for photosynthesis and carbon fixation (White et al. 2015).
The first shotgun metagenomes of Shark Bay mats (Ruvindy et al. 2016) were followed by 2 mm slices paired with chemistry (Wong et al. 2017) and 87 genomes reconstructed from the mat, including Asgard archaea, the closest known relatives of complex cells (Wong et al. 2018).
The first viral metagenome from a stromatolite (White et al. 2018) led to a new hypothesis: viruses may help decide whether a soft mat turns to stone (White, Visscher and Burns 2021). Read the hypothesis.
115genomes of uncultured microbes from 42 phyla, reconstructed from Shark Bay mats: the microbial dark matter (Wong et al. 2020).
Living microbialites survive in scattered places on every continent, from Antarctic lakes to Andean salt flats, and many of them are in trouble.
A reef-like band of thrombolites, listed as critically endangered under Western Australia’s Biodiversity Conservation Act and the federal EPBC Act after nutrients and salinity in the lake rose. A boardwalk lets visitors look without trampling (DBCA).
The largest freshwater microbialite occurrence known. Tourism and land-use change are altering its once nutrient-poor water, and people standing on microbialites damage them (PLOS ONE 2020; Goethe-Institut).
Protected within a World Heritage Area and a marine nature reserve, but not from warming and shifts in salinity. That is why baseline studies of its mats matter now (Reinold et al. 2019).
Richard Allen White III, UNC Charlotte
Metagenomes, genomes and viruses of freshwater and hypersaline microbialites.
Sites: Pavilion and Kelly lakes in British Columbia, Clinton Creek in the Yukon, Green Lake in New York, and Shark Bay with the Burns lab.
Pieter T. Visscher, University of Connecticut
The biogeochemistry of microbial mats, and how microbial metabolism turns a mat into rock.
Brendan P. Burns, UNSW Sydney
The molecular ecology and evolution of the microbial mats and stromatolites of Shark Bay.
