91ɫƬ

The shocking decline of Earth’s microbiome – and how to save it

Bacteria, fungi and other microbes, which are vital to life on Earth, were long thought impervious to threats endangering larger lifeforms. Now biologists are warning of a microbial extinction event

SCOOP up a handful of soil and you hold an entire ecosystem in the palm of your hand. That precious clod might not be much to look at with the naked eye, but it is teeming with life. A gram of soil contains around a billion single-celled organisms, including tens of thousands of different species, and if you could tease out the fungal strands, they would stretch for hundreds of kilometres. These are indispensable to life on Earth, including you and me. If they all died, we would soon follow.

They are dying.

For a long time, bacteria, fungi and other microbes were thought to be impervious to the agents of extinction wreaking havoc on larger organisms. They are so abundant and reproduce so quickly, the thinking went, that they couldn’t possibly be threatened. In recent years, however, microbiologists have come to question this assumption – and now they are sounding the alarm that microbe populations are in decline, possibly precipitously.

“We’re starting to see scary signals that there may be this large microbial extinction event under way that we barely noticed,” says , an ecologist at ETH Zurich in Switzerland.

When we think of biodiversity decline, we usually sweat the big stuff: plants, fish, reptiles, birds and mammals. But these are just the tip of the iceberg. All told, there are perhaps 7.7 million species of animal, around 80 per cent of which are insects and other arthropods, including arachnids and crustaceans. But there are at least 6 million species of terrestrial fungus and up to a trillion species of bacterium and archaeon, collectively known as prokaryotes. On top of that, there are about 200,000 species of complex unicellular microorganisms called protists, such as slime moulds. These latter two groups make up the majority of Earth’s biodiversity.

Microorganisms are not only remarkable for their sheer weight of numbers and diversity, but also for what they do. They are the main decomposers of organic matter. They form vital mutually beneficial relationships, or symbioses, with 90 per cent of plant species. And they – carbon, hydrogen, nitrogen, oxygen, phosphorus and sulphur. “The Earth microbiome provides an essential life-support system to our planet,” says Averill.

The first inkling that this system might itself be vulnerable came in 2007, when and , then at the Pierre and Marie Curie University in Paris, wrote a paper , first put forward in 1934, which suggests that when it comes to microbes “everything is everywhere”.

This posits that due to their minute size and vast abundance, microbes are universally distributed worldwide. Any regional variation is caused by environmental constraints, not by physical barriers to distribution of the sort that keep larger life forms confined to home ranges. Elephants, for example, cannot migrate to the Americas because crossing the ocean is impossible. Bacteria can simply blow across on the wind. If so, the idea goes, then there is always a vast reservoir of every species that can repopulate any place, any time.

Can bacteria go extinct?

Testing the cosmopolitan hypothesis has always been difficult, as failure to find a microbial species somewhere doesn’t prove it isn’t there. But there are plenty of reasons to doubt it. We know that the genomes of several species of bacterium vary depending on their geographic location – and that the genetic variation is greater the further away they are from each other. This suggests that these microbes have been evolving in isolation from one another with no genetic exchange.

Ditto fungi, many of which live dual lives as microscopic and macroscopic organisms. According to , a mycologist at Cardiff University, UK, a good example is the wood-decaying fungus Hyphoderma setigerum. It was once thought to have a global distribution, but DNA analysis has shown that it actually has nine subspecies with geographically distinct ranges.

The “everything is everywhere” dictum is no longer valid, says Boddy. “It really is not true. Not all microbes are everywhere. They have biogeography. In other words, they are found in certain parts of the globe.” That doesn’t mean that no microbial species are cosmopolitan, says Weinbauer, but it does suggest that biologists have been lulled into a false sense of security about the extinction-proofness of microbes.

Certain species have almost certainly already disappeared. Whenever an animal or plant goes extinct, it usually takes a retinue of microorganisms with it. “All the specific microbes living in the hair of the mammoth or the feathers of the dodo, all the specific microbes associated with the specific lice of these species, all their specific pathogens are extinct,” says Weinbauer. More recently, botanists in Brazil discovered six previously unknown species of fungus , Coussapoa floccosa, which until recently was thought to be extinct. If and when the last specimen dies, those fungi will disappear too.

The Carbon Community project in the Glandwr Forest in Wales. The sampling bags are specific to the microbiome and are samples gathered by the Crowther Lab during their visit in July 2022. The site photos all relate to The Carbon Community, where scientists from Crowther Lab and other organisations are studying microbiome restoration and the impact on tree growth. Photos are of a site, where microbiome restoration is being studied.
Microbe restoration is being tested in the Glandwr Forest in Wales, UK
The Carbon Community

Now, some 15 years on from what Weinbauer called his “quite speculative” paper, the evidence is mounting to suggest we are in the midst of an actual decline in the abundance and variety of microbes. “There is an emerging realisation that Earth’s microbial biodiversity is under threat,” says Averill.

Most of the evidence comes from soil fungi, many of which spend much of their life cycle as microorganisms, but also produce the bulbous fruiting bodies we know as mushrooms, toadstools, bracket fungi and the like. These are easy enough to spot, so they are often used as surrogates for the state of forest biodiversity, especially of the underground mycorrhizae – fungi that form symbiotic relationships with tree roots, taking sugars and supplying plants with water and mineral nutrients in return.

As early as the 1980s, there were signs that all was not well in the underworld. Eef Arnolds at what is now Wageningen University in the Netherlands compared historical records of the fruiting bodies of mycorrhizal fungi spotted on field trips in that country. Between 1912 and 1954, the average number of species seen per trip was 71. By the mid-1980s, that had declined to 38. Similar falls were recorded in Germany by the indefatigable mycologist Helmut Derbsch, who sampled the same piece of woodland near Saarbrücken 3500 times between 1950 and 1985. Even steeper falls were seen elsewhere.

All told, says Averill, the species-level diversity of ectomycorrhizal fungi has declined by 45 per cent across Europe over the past century.

Arnolds put the decline down to two factors: air pollution and intensive forest management, which removes fungus food – dead wood and leaf litter – and replaces native trees with non-native ones. One later study in Sweden found that the abundance of wood-decaying fungal species was there.

Microbial diversity in decline

“As we lose habitats, what we’ve learned from all these different studies is that we’re losing all of this other associated microbial biodiversity,” says Averill. Habitat loss can sometimes have a surprising cause. The decline of the now-endangered fungus Poronia punctata, for example, mirrors the rise of car ownership – but not because of pollution. Its preferred habitat is horse dung, which is much less abundant today because of changes to the way we get around.

The problem is that it is nigh-on impossible to confirm the demise of a microbial species. “It’s remarkably difficult to prove the extinction of any organism, and when you start talking about microorganisms, it’s even more challenging because most species are undescribed,” says Averill. “But we’d be surprised if those extinctions were not happening.” Boddy shares that view. “As with plants and animals, mass extinctions of fungi are likely to occur, but when they do, many will be unrecorded, as so many species are still unknown,” she says.

What we can see is definite evidence not only of a decline in abundance, but also homogenisation, where the same common fungi dominate soil ecosystems ever more and the exotic ones dwindle and disappear. The same is seen in larger organisms, where rare, endemic animals are increasingly being displaced by rats, cats and pigs. As for the estimated 5×1030 prokaryotic cells on Earth, we just don’t have the data. And it’s a similar story for viruses.

Where the data exists, it points to a widespread problem. “We are focused on mycorrhizal fungi, that’s where most of the expertise and interest lies, but we see bacteria experiencing this homogenisation too,” says Averill. “As we’ve used more and more DNA-sequencing technology, we’re seeing this intense homogenisation. All of a sudden, all of the same organisms are showing up and all of the rare organisms that make these habitats microbiologically distinct start dropping out of the species pool.”

On top of that, multiple studies over the past few years have concluded that microorganisms are sensitive to the same sorts of pressures that are threatening larger organisms: habitat loss, invasive species, pollution and wildfires.

The consequences of a large microbial extinction event would be disastrous. In 2020, when a widely reported study demonstrated a precipitous decline in insects, ecologists warned of potentially devastating impacts. Insects are key players in most ecosystems, providing food for other species, recycling nutrients, disposing of dung, controlling pests and pollinating plants. A 2019 review paper on insect decline warned that “the repercussions this will have for the planet’s ecosystems are catastrophic to say the least”. A microbial apocalypse would be even worse.

“Don’t get me wrong here, but if all mammals were wiped out, that wouldn’t have very much effect on the functioning of most ecosystems,” says Boddy. “But bacteria, archaea and fungi are a totally different matter. If we lost a whole group, it would be disastrous because ecosystem function depends on them. You can’t overemphasise the importance of microbes.”

Boddy likes to quote at Newcastle University, UK, who in 2006 : “If the last blue whale choked to death on the last panda, it would be disastrous but not the end of the world. But if we accidentally poisoned the last two species of ammonia-oxidizers, that would be another matter. It could be happening now and we wouldn’t even know…”

All moral rights asserted. Recolouring or alteration of the image is prohibited without permission. Coloured scanning electron micrograph (SEM) of a freeze-fracture preparation of a grass plant root with endomycorrhiza (light grey). A mycorrhiza is an association between a soil fungus and the roots of a vascular plant. The majority of vascular plant roots are mycorrhizal. Endomycorrhizal fungi grow within cell walls of the root. Both organisms benefit from this association. The fungus is able to access nutrient forms unavailable to the plant, process them and pass them on to the roots. The mass of fungal hyphae also provide a large surface area for the uptake of water and minerals. The fungus receives carbon compounds that the plant produces via photosynthesis. Magnification: x700 when printed at 15cm wide.
The root of a grass plant covered in mycorrhizal fungi (grey), which is in decline across Europe
EYE OF SCIENCE/SCIENCE PHOTO LIBRARY

This dearth of knowledge is a major barrier to assessing the state of Earth’s microbiome. Of the 6 million or so species of terrestrial fungus, only 140,000 have been fully characterised, says Boddy. “There will be microbes, certainly fungi, going extinct all the time. And we probably haven’t even discovered them yet.”

Fortunately, it is unlikely to be too late to arrest and reverse the decline, though we can’t afford to be complacent. The first step is to map and conserve what is left. “We need to get a handle on what’s there,” says Averill. “By combining DNA-based microbial surveys from around the world, we can start to get pictures of where microbial biodiversity is highest and most intact and where it’s most degraded. And that can act as a baseline we can continue to monitor and use to identify places that need to become conservation priorities.”

To that end, various initiatives have started documenting the soil microbiome, and another three – the , and (Society for the Protection of Underground Networks) – are compiling the data.

Step two is to restore. “We’re witnessing a global movement in restoration and reforestation, trying to bring back natural ecosystems,” says Averill. “But when we go and plant a tree, we rarely think to plant the associated microbiome. So we’re going to work with more and more groups where we start actually moving microbes, doing active microbiome restoration as part of reforestation projects.” Averill and his team analysed the results of 27 restoration experiments that also added wild microbiomes and found that plant growth increased by an average of 64 per cent versus plots that weren’t seeded or that used commercial mycorrhizal solutions. “There seems to be something special about the wild, native microbiology,” he says.

Restoring the underground microbiome

Based on this research, Averill and some of his colleagues have founded a public benefit corporation called that aims to improve the productivity of forestry projects and help tackle climate change by restoring the underground microbiome.

Its model has already been , where researchers planted 25,600 trees across 11 hectares of farmland. Half were native broadleaf species, including alder, aspen, birch, cherry, oak and rowan. The other half were Sitka spruce, typical of commercial monoculture plantations. Some of the trees were planted as normal, others had their roots inoculated with a commercial conifer mycorrhizal solution, while those in a third group were planted with a spadeful of fresh soil from a nearby forest.

“Using DNA technology, we can identify forests with great soil microbiology and then use that soil to inoculate at the time of planting,” says Averill. It is early days, but there are some encouraging signs that such soil transplants work. “We’re already seeing the trees growing faster where we’ve done these inoculations,” says Averill. The next step is to try the technology out in a commercial loblolly pine plantation near Athens, Georgia.

There are also stirrings in the corridors of power. In 2021, the International Union for Conservation of Nature pledged to recognise fungi as the equals of animals and plants in terms of conservation need, and revised its slogan to “fauna, flora and funga”. But it isn’t enough. “Other microbes still really aren’t considered,” says Boddy.

As our understanding of extinction risk has cascaded down the levels of biological organisation, from plants and large animals to insects and finally microbes, it seems we really are hitting rock bottom. According to Averill, this is our final wake-up call. “A functioning Earth without a functioning microbiome is nearly unimaginable.”

Graham Lawton is staff feature writer at New Scientist

Topics: Biodiversity / Extinction / Microbiome