Last week I was very fortunate. I had the opportunity to focus my attention on putting life on Earth in perspective. It was a welcome respite considering these trying times. Almost one year ago, thanks to Nassos Typas, I received an invitation to speak on microbial diversity at the European Molecular Biology Laboratory (EMBL) in Heidelberg. The occasion was to be their 21st Science and Society Conference entitled "Our house is burning: scientific and societal responses to mass extinction." The conference should have been last week but, of course, there was no trip to Heidelberg. Instead, it went virtual. But it still provided me with a wonderful opportunity for thinking. Let me share some of those thoughts with you.
By using the phrase "our house is burning" the organizers managed to convey the sense of horror of watching our property destroyed by fire. It is impossible to not be shaken by that mental image. Since the house being referred to is planet Earth, the feelings that emerge become ever more shocking. To alleviate this shock, I found it extremely useful to put different life forms in perspective in terms of their relative sizes, numbers and their time of residence on the planet.
This is an image of our house, magnificent planet Earth, in what I consider one of its most stunning perspectives, a portrait from space. The very fact that such images can be captured speaks volumes as to what humans can accomplish. And humanity's never-ending search for meaning is epitomized by our desire to explore, even sending crafts out to space, leaving Earth far behind, a "mote of dust suspended in a sunbeam," Carl Sagan's Pale Blue Dot. But humans also caused many of the problems that the planet now faces, global warming and massive loss of biodiversity prime among them. How does an organism, whose dimension is about one meter, have such devastating effects on a planet whose diameter is 107 times larger? These days that's not too hard to imagine, we are all aware that an entity 10-7 the size of a human easily wreaks havoc on its host. Welcome to the Anthropocene, the epoch in the natural history of Earth characterized by noticeable human impact on ecosystems and geology. Lest you think – as some proponents do – that the Anthropocene started with the Trinity test, I remind you that the extinction of South American megafauna some 12,000 years ago coincided with the arrival of Homo sapiens.
The conference overview statement started by putting the current loss of biodiversity in the context of Earth's history: "There have been five mass extinctions in Earth's history, but are we already in the midst of a sixth? At least one million animal and plant species are currently threatened with extinction, many within decades – a rate unprecedented in human history." But what about the microbes? Did they suffer great declines in the prior five mass extinctions? Are microbes declining in the midst of a sixth? (Do these sound like Talmudic Questions?)
To me the microbes are the most foundational of all life forms. Though largely invisible as individuals, they play and have always played key roles in the functioning of all ecosystems. So much so, that I do not think of this planet as 'our' house, rather it is the microbes' house. Homo sapiens only recently stepped in as a guest and, mind you, thus far we have been far from an ideal guest. We can only hope that this improves in the near future.
What have been the dynamics of microbial populations along Earth's history? Answering this question is not an easy task. Over the long run, the microbial fossil record is poor compared to that of plants and animals. Plus, assessment of current overall changes is made difficult due to the gargantuan microbial cell population and diversity. There are some 1030 cells and upwards of 1012 species (though the very concept of species is debatable, as we discussed here before).
Let's first have a look at the so-called "Big Five" mass extinction events. The first happened 440 million years ago, the fifth, 65 million years ago. From the fossil record, the percent of species lost range from 75−95%. The causes were usually planetary cooling and volcanism. The fifth one also involved the Deccan Traps and the now famous asteroid collision that created the Chicxulub crater, and famously led to the demise of the dinosaurs, among others. When it comes to microbes, there's no direct evidence for their demise during these five periods. However, through indirect approaches, investigators have speculated both ways. In 1998 Dykhuizen argued that bacteria intrinsically have very low extinction rates and very high speciation rates. These attributes would render them resistant to mass extinction. In contrast, in 2007 Weinbauer and Rassoulzadegan speculated that whenever an animal or plant species becomes extinct, many of the host-associated microbial species follow along. But would this have led to mass extinctions? A more recent (2018) paper by Louca et al. attempts to answer that question. The authors developed methods to analyze the phylogenies of nearly half-million bacterial lineages and determined the fraction of extant bacterial diversity missing from the phylogenies. From their results they conclude: "Most bacterial lineages ever to have inhabited this planet are estimated to be extinct. Our findings disprove the notion that bacteria are unlikely to go extinct, and provide a valuable perspective on the evolutionary history of a domain of life with a sparse and cryptic fossil record." Importantly, while they argue for bacterial extinctions, they conclude that their "findings suggest that, during the past billion years, global bacterial speciation and extinction rates were not substantially affected during the mass extinction events seen in eukaryotic fossil records."
Let's now put those mass extinctions of plants and animals in the perspective of the entire natural history of the planet. Looking at my rough timeline several features stand out. First, Homo sapiens just recently entered the scene. Second, the five mass extinction events I've discussed are relatively recent because, after all, plants and animals were not around for the vast majority of Earth's history. Third, there were only microbes for the first three billion years of evolution.
By the time plants and animals first evolved, the planet was replete with microbes. And they had been responsible for one of the most remarkable changes in the planet's history: The Great Oxygenation Event (GOE). Not long after the first microbes appeared, some evolved photosynthesis, the capacity to harness the energy from light to convert CO2 into sugars. A by-product of the reaction was the production of highly reactive oxygen gas. Initially, most of the oxygen reacted with iron in seawater to form iron oxides on the ocean bottom, giving rise to what we now know as "banded iron formations." But eventually oxygen began to accumulate. This poisoning of the atmosphere with such a reactive molecule must have led to the greatest mass extinction of all time, but it took several hundred million years to unfold. That gave time for life on the planet to adapt. Two key evolutionary steps related to the presence of oxygen occurred as a consequence of the GOE that changed our planet forever. First, bacteria evolved the capacity to dump electrons onto oxygen and thus generate energy much efficiently. For the first time there were aerobic respirers. Subsequently, an archaeon somewhere became entangled and eventually fused with one of these aerobes and gave rise to LECA, the last eukaryote common ancestor. The rest is… well, natural history.
To end, let's fast forward to the present, to the midst of the "sixth extinction" and inquire whether microbes are suffering the same fate as so many of the plants and animals. To address this, I will sidestep the issue of extinction. This I do for two reasons. The immensity of microbial biodiversity and the difficulty in defining a species makes it almost futile to determine if specific lineages have become extinct "forever." More importantly, as Ceballos et al. have argued, focusing on species extinctions "leads to a common misimpression that Earth’s biota is not immediately threatened, just slowly entering an episode of major biodiversity loss." It is far better to determine if population sizes and ranges are affected. For plants and animals, the evidence is stunning. In their words: "Dwindling population sizes and range shrinkages amount to a massive anthropogenic erosion of biodiversity and of the ecosystem services essential to civilization. This 'biological annihilation' underlines the seriousness for humanity of Earth's ongoing sixth mass extinction event. Sadly, similar biological annihilation is observed among microbes. Here are just a couple of examples: Global phytoplankton has declined dramatically over the past century and the diversity of the intestinal microbiota of "westernized" humans is about half that found in previously uncontacted Amerindians. Is the situation bleak beyond repair? I don't think so, but then I consider myself an optimist. I believe if microbial ecosystems are allowed to recover, they will. It's just that humans need to take dramatic actions. We need to continue to pursue aggressive actions as communities, as countries, as a world, even when some leaders insist on turning a blind eye to the catastrophe. And as an individual I'll continue with lessons that have been hammered home by the pandemic: drive less, fly less and eat less meat.