Making Eden

by David Beerling

  What, if any, is the broader significance of mycorrhizal fungi for weathering

  rocks? Answering that question is crucial to the business of determining whether

  these microbes have been playing a hidden role in driving global change over hun-

  dreds of millions of years of Earth’s history. Some insights came from field trials exploiting the superb tree collections in the Westonbirt National Arboretum,

  Gloucestershire in the UK. Situated in a historic landscape that has survived since Victorian times thanks to careful management by the Forestry Commission,

  Westonbirt is a living collection of over 3000 different trees.34 When combined

  with a management team agreeable to our undertaking scientific field trials, the

  site provided us with the perfect opportunity to investigate rock grain weather-

  ing beneath trees whose roots are bound in tight symbiotic alliance with mycor-

  rhizal fungi. The simple trick of incubating uniform-sized grains of silicate

  rocks in mesh bags buried in soils beneath the trees proved key. By carefully

  selecting the size of the mesh, fine tree roots were excluded but fungal threads

  could enter, colonize, and weather the test rock grains. In other words, incubating the rock grains in this way allowed us to isolate the actions of mycorrhizal fungi.

  The secret world of microbial weathering beneath the Westonbirt trees soon

  revealed itself. The fungal partners of the gymnosperm trees Metasequoia and Sequoia, selected as the closest modern analogues to Devonian forest trees, proliferated in mesh bags containing basalt grains but not in those containing other less easily

  weatherable grains of granite or quartz.35 Such targeted fungal proliferation reflects a tightly regulated self-reinforcing or positive feedback mechanism operating between the two groups of organisms involved—trees and fungi. As the fungi colonize the

  basalt grains and pass the weathered nutritious elements back to their host tree roots, the tree in return ups its provision of photosynthate to the fungus, enabling it to proliferate, do more weathering, and capture more nutrients. Now consider the reverse

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  situation: how the feedback loop is shut down if fungi colonized unreactive rock

  grains. A lack of nutritious elements to pass back to the host tree means no extra carbon reward provided by the roots, slowing fungal growth. Mineral flakes recovered from the mesh bags also confirmed that fungi really do seem to be tiny trench dig-gers. The size and shape of the trenches measured on the flakes perfectly matched those of fungal hyphae as they etched their way across the mineral surface.36

  With mycorrhizal fungi becoming recognized as possible agents of weather-

  ing, the focus turned to explaining how they achieve this feat. The answer comes

  from thinking about the flow of carbon energy between the plants and fungi. The

  energy flux is really a flow of sugars synthesized by photosynthesis that starts life in the tree canopy, from where it moves downwards into roots to support the pervasive growth of fungal networks in the soils below. Rock-eating microbes, it

  turns out, have an appetite for weathering that varies in proportion to the carbon-energy flux they receive from host trees.37

  But how is it that cotton-wool-like fungal filaments can dissolve rock and min-

  eral grains? The answer is through a variety of metabolic tricks, one of which

  involves bonding themselves tightly to mineral grains by special sticky proteins.

  This enables them to generate massive internal pressures—typically 4000–10 000

  times higher than atmospheric pressure at sea-level38—to ‘inflate’ the fungal filament, and drive their exploratory growth. Such pressures may even be an evolu-

  tionary adaptation for penetrating rock surfaces and, in the case of pathogenic

  fungi, plant tissues. By bonding tightly to the surface of the mineral, the fungus can generate spectacular downward forces that mechanically fracture rock grains.

  For good measure, they combine this mechanical pressure with an acid bath

  treatment, thanks to the extremely high metabolic rates of the hyphae, generating carbon dioxide, the waste product of aerobic respiration, which acidifies the aque-ous soil solution in which they live. Acidification is highly localized by rapidly proliferating hyphae. Exuding streams of hydrogen ions during nutrient uptake,

  they weaken the already pressured mineral surface, causing it to split and frac-

  ture. Every split and fracture opens up new faces for the chemical weathering

  reactions to proceed, hastening destruction. Countless millions of hyphae are,

  unnoticed, eating their way through countless rock grains in soils of the world,

  supported by carbon supplies delivered from the trees above ground.39

  Bringing mycorrhizal fungi into our picture of events in the Devonian,

  adds a new link to the chain of cause and effect involving the soil nutrient,

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  phosphorus.40 Phosphorus is an essential element for all forms of life, which need it for making DNA and cell membranes, amongst other things. In the early stages

  of soil formation, it is provided by the weathering of the mineral apatite because most of the phosphorus in the Earth’s crust (over 95%) is locked up in apatite, with far smaller amounts occurring as inclusions in igneous rocks. On land, apatite

  stocks are being slowly but progressively depleted by weathering. Stocks are only recycled when plate tectonics uplifts buried rocks containing apatite or when volcanic eruptions at plate boundaries spew out huge amounts of fast-weathering

  basalt. Apatite depletion on land means that, in the long run, the productivity and biomass of the trees declines as they exhaust rock phosphorus supplies.41 Consider how this might have played out with the arrival of trees and then forests of trees in the Devonian. As early trees and forests evolved into the major forms, including those uncovered by Berry, Stein, and colleagues, what better way to meet their growing demand for phosphorus than by teaming up with mycorrhizal fungi that

  are highly adept at mining it from apatite in soils? It is easy to imagine these early forests expending carbon energy to support mycorrhizal fungal partners in

  return for obtaining access to the phosphorus supplies necessary for running

  their metabolism and building biomass.

  At this point, however, we should acknowledge that evidence for fossil mycor-

  rhizal partnerships in the roots of trees forming Devonian forests is lacking. We should be mindful of the limited nature of the fossil record of these trees and its generally poor quality of preservation. Recall that forests like those in Gilboa

  have little of the original anatomy remaining. Here, the dictum ‘absence of evi-

  dence is not the same as evidence of absence’ is apposite. By the time of the

  Carboniferous, arborescent lycopsids, which dominated the extensive tropical

  swamplands and rose to heights of over 30 metres, were mycorrhizal, as we

  know from well-preserved fossilized strap-like root appendages preserving

  arbuscules and other diagnostic features of the fungi. These giants of the past

  have since become extinct but we also know that all of the extant gymnosperm

  groups that originated at least 300 million years ago (including cycads, ginkgo,

  and others) form mycorrhizal partnerships that facilitate the release of phos-

  phorus from apatite.42 There is also the constancy of mycorrhizal alliances of

  trees since those far-off days of the Carboniferous because all later-evolving tree groups have roots tightly bound into associations with symbiotic fungi. So it is

  simply inconceivable to imagine Devonian trees as being any different to modern

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  trees in terms of rely
ing on fungal symbionts to fulfil their nutrient demands as they evolved progressively larger stature.

  A revised hypothesis explaining how the rise of Devonian forests bioengin-

  eered Earth’s climate as they ‘greened’ the continental land surface might, then, look something like this. As trees with bigger and architecturally more complex

  rooting systems evolved, they pumped more carbon energy below ground, fuel-

  ling the rock mining by roots and mycorrhiza for phosphorus and other essential

  elements needed to meet the rising demands for synthesizing more tissues. These

  activities, in turn, acidified soils and increased the bio logically driven weathering of rocks. The carbon fluxes involved were likely enormous. Forests and grasslands of the modern world direct a carbon-energy flux estimated to be equivalent

  to around six times our annual electricity production from burning fossil fuels.43

  Or, put another way, three to seven orders of magnitude greater than the kinetic

  energy generated by tectonic uplift tradition ally thought to regulate the global biogeochemical cycling of elements over time.44

  Viewed in the light of such mind-boggling numbers, it starts to become clearer

  how the arrival and spread of forests through the Devonian might have bioengin-

  eered global climate, ramping up the carbon-energy flux pumped into soils via allocation to roots and mycorrhiza to influence rock weathering and atmospheric

  carbon dioxide sequestration.45 We can capture nutrient effects simply by adding an extra step in our logical sequence. Nature abhors destabilizing or self-reinforcing (positive) feedback loops and yet by doing this we find one that looks like this: bigger trees → deeper roots → faster weathering → greater nutrient release → bigger trees.

  PEAK PHOSPHORUS?

  -

  Humanity, like the emerging forests that ‘greened’ the continental land surfaces, has a huge and growing demand for phosphorus. We rely on rock phosphate

  that formed 10–15 million years ago for supplies to make fertilizers that support modern agricultural production. Unlike nitrogen fertilizers synthesized industrially with the Haber–Bosch process, we are unable to synthesize phosphorus

  in the lab. Like time itself, phosphorus is non-renewable. There is no substitute.

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  Yet excess phosphorus is being wasted as it flows from fertilizers to water-

  courses and coastal oceans, fuelling intense algal blooms that deliver pulses of

  organic matter to sediments. Microbial decomposers consume dissolved oxy-

  gen, creating gigantic ‘dead zones’ in the coastal oceans—affecting over 250 000

  km2 in 2008.46 The anthropogenic black-shales of the modern world that will

  eventually form around the coasts will tell our story to future gener ations of

  geologists reading humanity’s footprint on the sediments of the planet.

  Meeting the agricultural demand for fertilizers saw global extraction of

  phosphate rock triple since the end of the Second World War.47 Costs rise as the

  quality of phosphate rock reserves declines, raising the question: are we

  approaching peak phosphorus production, a time when we are consuming it

  faster than we can economically extract it? Peak production might be on the

  horizon within a few generations, but an accurate timeline depends on assess-

  ing the quantity remaining in the ground, and the extent we recycle. Gauging

  reserves is dependent on voluntary provision of data and old geological assess-

  ments.48 Currently, the four top countries thought to control more than 85% of

  known phosphorus reserves, are Morocco, China, Algeria, and Syria, with

  Morocco in the driving seat. By contrast, a dozen members of OPEC control

  80% of the world’s oil reserves.

  There is no ‘quick fix’. We must face up to the prospect of recycling

  phosphorus from human waste, as the French poet and author Victor Hugo

  (1802–1885) highlighted in Les Misérables:

  Science, after having long groped about, now knows that the most fecundating

  and the most efficacious of fertilizers is human manure. The Chinese, let us

  confess to our shame, knew about it before us . . . If our gold is manure, our

  manure on the other hand, is gold.

  Toxins, drugs, and heavy metals rule out the use of untreated sewage, but

  the idea is getting a modern resurrection, with companies converting ashes

  from the combustion of sewage sludge in incinerators into high-quality,

  phosphate-rich fertilizer fit for crops.49 Adapting agricultural management

  practices to reduce phosphorus demand is also needed.50 In 1938, US President

  Franklin Roosevelt said it was ‘high time for the Nation to adopt a national

  policy for the production of phosphates for the benefit of this and coming

  generations’.51 Seventy-five years later, we are still searching for long-term

  solutions to the phosphorus problem.

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  The question raised by uncovering potentially destabilizing climate feedbacks

  in explaining the role of trees and forests in air conditioning the planet through the Devonian is this: why has Earth not experienced runaway cooling since they

  appeared on the continents? A system of checks and balances has to be operational in stabilizing changes in atmospheric carbon dioxide levels to have prevented

  Earth’s climate spiralling out of control. Geochemists believe that these stabilizing (or negative) feedback loops constitute a planetary thermostat, involving

  weathering, carbon dioxide, and climate.52

  To imagine how the thermostat might operate, consider this scenario. Suppose

  atmospheric carbon dioxide levels rose due to a massive and prolonged episode

  of volcanic activity. This would drive a warmer climate, due to an enhanced

  greenhouse effect, and a wetter climate, by causing a more vigorous precipita-

  tion cycle. Both features accelerate chemical reaction rates of rock weathering,

  which remove carbon dioxide from the atmosphere and cool the planet. The

  thermostat also operates in reverse if atmospheric carbon dioxide levels are falling, thereby slowing weathering and allowing carbon dioxide to build up.

  Suppose, for example, the uplift of major mountain range exposed large amounts

  of fresh unweathered rocks to the atmosphere. These rocks can now react with

  mildly acidic rainwater to remove carbon dioxide from the atmosphere as they

  undergo weathering. The rise of the Himalayas is a good example of such a

  tectonic event. It is linked causally to a global decline in the atmospheric carbon dioxide concentration and climate cooling, as witnessed by the ensuing glaciation of Antarctica, and a slower weathering regime.53

  Of course, there are more processes involved, and for rock weathering to oper-

  ate as a climate feedback the Earth must be sufficiently tectonically active to

  ensure an adequate supply of fresh rocks and minerals. In this context, the dramatic 90% drop in atmospheric carbon dioxide caused by the rise of trees through the

  Devonian is analogous to the uplift of a massive mountain range. It switched Earth into a mode of accelerated weathering, sequestering atmospheric carbon dioxide,

  and cooling the climate to resist further weathering. Indeed, there was also the uplift of an equatorial mountain range in the Permo-Carboniferous that may have reinforced the effects of trees in cooling the planet. Conversely, its later destruction may also have contributed to putting the brake on weathering, checking further cooling.54

  Shifts in the balance between volcanoes adding carbon dioxide to the atmos-

>   phere, and rock weathering slowly removing it, are reflected in Earth’s atmospheric carbon dioxide history, as reconstructed from a variety of fossil materials for

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  Age (millions of years ago)

  Year A.D.

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  2 1

  1,000 1,500 2,000 2,500

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  Wink12K

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  Future carbon

  2,000

  dioxide

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  pathways

  (p.p.m 2 500

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  200

  Ice core Ice core

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  Age (millions of years ago)

  Age (thousands of years ago)

  Figure 24 Earth’s atmospheric carbon dioxide (CO2) history over the past 420 million years plotted alongside possible future pathways of increases in comparison. Notice the apparent minimum threshold or lower limit that has prevailed over the past 20 million years. Dashed line indicates the current average CO2 concentration (405 p.p.m. in 2017) the last half billion years (Figure 24).55 Careful inspection of this impressive reconstruction reveals a curious feature—when the atmospheric carbon dioxide

  concentration falls, it seems to bump up against the same minimum value, over

  and over again.56 Over the past 24 million years, in particular, carbon dioxide

  levels have flat-lined, even, surprisingly, during major mountain-building epi-

  sodes like the uplift of the Southern Alps in New Zealand and the Andes.

  According to the geochemists, the production of huge quantities of fresh rock

  during these tectonic upheavals should have enhanced weathering and sucked

  carbon dioxide out of the atmosphere. Yet for some reason, it stayed put. If the

  reconstruction is valid, the pattern suggests the Earth system may have a built-in minimum atmospheric carbon dioxide concentration. The question is: do the

  mechanisms of this strange phenomenon extend beyond the imaginations of

  hard-rock geochemists?