In the 1930s, Alfred E. Treibs characterised the structure of metalloporphyrins in rocks and oil, revealing their similarities to and ultimately proving their origin from chlorophyll molecules in plants. From that the field of biomarker geochemistry was born, a discipline based on reconstructing Earth’s history using the molecular fossils of the organisms that once lived in those ancient lakes, soils and oceans.
Most biomarkers are lipids – or fats – although there are exceptions such as the porphyrins. Lipids are ideal biomarkers because they have marvelous structural variability, recording in their own way the tree of life and the adaptation of that life to the environments in which they live(d). And they are also ideal, because they are preserved, in sediments for thousands of years and in rocks for millions, often hundreds of millions and in some cases billions of years.
The classical way in which we use these biomarkers is to exploit those subtle structural changes as a record of environmental conditions – using the number of rings or branches or double bonds as a microbiological record of ancient temperatures or pH. We also use them to identify the sources of organic matter to ancient settings, helping us to characterise an ancient lake or sea or documenting the biotic response to a mass extinction.
They can even record the evolution of life. The rise and diversification of eukaryotes, the Palaeozoic colonisation of land by plants, the Cretaceous emergence of the angiosperms, the Mesozoic rise of red algae and the Cenozoic rise of certain coccolithophorids are all documented in the molecular record.
But that record also documents moments of profound weirdness in ancient oceans, transient events in which some ancient organism appeared, dominated the seas and thus the sedimentary record, and then disappeared, taking with them a suite of biosynthetic machinery.
The Jurassic Ocean
Take for example, the ancient Kimmeridge Sea, which covered much of the UK during the Jurassic about 155 million years ago and within which many North Sea oils were deposited as well as the magnificent sedimentary sequences of Kimmeridge Bay.
Within the archived sediments of this ancient basin, we observe many of the biomarkers for common life that we’d find in any sediment from the past 600 million years: eukaryotic-derived steranes (from sterols, such as cholesterol, which occur in every plant and animal) and bacterially-derived hopanes (from compounds similar to sterols but present only in Bacteria). But we also find very odd compounds, unusually-branched linear isoprenoids. The isoprenoids, compounds constructed of the five-carbon atom unit isoprene, are not odd; in fact, steranes and hopanes are just linear isoprenoids folded into rings, and the membrane lipids of the third domain of life, the Archaea, predominantly comprise linear isoprenoids. More on them below.
But the isoprenoids from some sedimentary horizons deposited in the ancient Kimmeridge Sea have extra branches or missing branches, revealing an assembly from smaller molecules in a manner unlike any organism on Earth today.
In those horizons, they eclipse all other biomarkers in abundance, indicating that these ancient organisms did not just persist at the fringes of life, an idiosyncrasy in a complex ecosystem, but were one of the dominant organisms.
And then they disappeared, taking these peculiar lipids with them.
An Archaeal Event in the Cretaceous
Deep in the Cretaceous, near the boundary between the Aptian and Albian Ages, about 110 million years ago, organic-rich sediments were deposited across the North Atlantic Ocean. The event is called Oceanic Anoxic Event (OAE) 1b. Such events are not uncommon, especially in the Cretaceous when combinations of algal blooms, restriction of ocean circulation and depletion of deep ocean oxygen facilitated the burial of the organic matter (that in many cases became the oil and gas that fuels the Anthropocene). But unlike earlier and later organic burial events, this event was not an algal event; it was not a plant event.
This was an Archaea event.
Archaea are ubiquitous on the planet, but rarely do they dominate, instead ceding the modern Earth to the plants and Bacteria. Their hardy physiology allows them to dominate in very high temperature geothermal settings and they are uniquely adapted to a handful of ecosystems. Some Archaea, those involved with the oxidation of ammonia, also appear to dominate in parts of the ocean, but only in scarce abundances, representing a significant proportion of the biomass only because other organisms find it even more challenging to eke out an existence in that sunlight-starved realm.
But 110 million years ago not only did they dominate, they dominated in a way that led to the deposition of thick layers of archaea-derived organic matter on the seafloor. We know this because nearly all of the organic matter – analysed through the lens of multiple analytical techniques probing the various pools of sedimentary organic matter, with names like bitumen and kerogen, maltenes an asphaltenes, saturates, aromatics and polars – are all dominated by compounds diagnostic for the Archaea.
But OAE1b was evidently not merely a brief explosion of the same Archaea that thrived at much lower abundances prior to and after it, and thrive at low abundances even today. No, this event included Archaea that biosynthesised subtle variations of classical Archaeal lipids, variations restricted -as far as we know – to this single event in all of Earth history.
Compound I from the figure above might not look that special; it takes a keen eye to distinguish it from Compound II below it. But like the unusual lipids of the Kimmeridge Clay Formation, it is apparently restricted to (and abundant during) only this one event.
These are weird biomarkers and that is why we love them. They prompt us to ponder the organisms that made them – and how and why? And this prompts further questions that are perhaps more fascinating and profound, and not just the interest of organic geochemists.
Why have no other organisms chosen to make them? Are these lipid simply an accident of phylogeny? Or are these a specific adaptation to the environmental and ecological needs of a particular moment in time, in a particular ocean basin? And that is both enigmatic and beautiful. It speaks to the rapid emergence and then the casual discarding of a biosynthetic pathway and the associated enzymatic machinery.
And surely that must say something of the organisms that have produced them. Because these weird and unique biomarkers also reveal the expansion and disappearance of the microorganisms that made them, organisms comprising not just a truncated branch on the tree of life but a branch that what was, for a brief while, thick and thriving. And now gone.
But as fascinating as these microbiological events are I am even more curious about those that we have we missed? Most life does not make such weird and singular lipids, relying on similar biomolecular solutions to similar ecological needs. Consequently, I suspect that there are many cryptic microbiological evolutionary events, invisible to the molecular fossil record. And by extension, are these simple organisms – the single-celled bacteria, archaea and microalgae – as primitive and eternal as we assume? Or is Earth history replete with exotic microbiological events – a multitude of failed experiments or singular innovations appropriate only for a moment in time – and then rendered invisible even to organic geochemists because they have not been signposted by a peculiar lipid?
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