History, according to the heartfelt judgement of a young scholar in Alan Bennett’s marvellous play The History Boys “[is] just one fuckin’ thing after another.” Biology is a bit like this, because evolution works with a single set of raw materials within the constraints imposed by the planet’s environmental conditions. Every cell is surrounded by a lipid membrane, encodes its information in nucleic acids, and manufactures proteins. Every cell is powered like a battery and uses the electrical current carried by ions to import food, signal to its neighbours, and excrete waste products. At the same time, birds are different from bacteria because biomolecules can be arranged in an immense number of combinations, and sufficient time has elapsed to shuffle the molecules to suit every accommodation on earth. There is a tussle here, between the picture of life drawn from the viewpoint of thermodynamics and the experience of nature afforded anyone walking in the woods or looking at a compost heap with a hand lens. Both views are correct: sameness at the level of life’s essence, variety in its manifestation.

Human comprehension of biology has always been distorted by our innate occupation with organisms that are roughly the same size as us, and scientists have believed, until very recently, that organisms of our size are the most important ones for understanding life. Before the seventeenth century, the obvious impediment was our blindness to things smaller than fleas. The slight magnification of insects by Galileo’s friends at the Accademia dei Lincei – using a modified telescope – was nonetheless revelatory and soon, with the evolution of the microscope, the universe of microorganisms was laid bare. Prospects for intellectual recalibration began with these inventions, but the microscopic didn’t bleed into popular consciousness until the link between germs and disease was established in the nineteenth century. During my lifetime we have learned that a far greater repository of biological diversity exists among the unicellular organisms and the viruses than we find throughout the animal and plant kingdoms. Yet even in the twenty-first century the majority of professional scientists are preoccupied with macrobiology. This is a problem for science and for our species.

Ecology cannot be taught any more without considering the importance of microorganisms, and this is a very good thing indeed.”

Ecologists have exemplified this tension between the macro and the micro of biology. For more than 60 years, ecologists have been interested in understanding how the biodiversity within different ecosystems is determined. Throughout the twentieth century, the number of plant and animal species was viewed as the primary metric of biodiversity. Plant ecologists looked at the number of plant species as well as the distribution of different types of plants in particular settings, and developed models of productivity to explain how ecosystems worked. Animal ecologists, on the other hand, pursued similar ideas about animal diversity, and a few of the more interdisciplinary researchers blended these concerns by looking at the effects of herbivores on plant productivity. Microorganisms were included in the standard models of nutrient flow, with fungi, for example, listed as decomposers in models of the carbon cycle. The emphasis, however, was always on plants and animals. Until quite recently, plant and animal ecologists ignored microbes. Microbial ecology was a separate and specialised endeavour.

This is a broad-brushstrokes picture of ecology, but few ecologists of my generation will dispute the contention that the zeitgeist has changed in the last 20 years. Ecology cannot be taught any more without considering the importance of microorganisms, and this is a very good thing indeed. By introducing microbes into models of terrestrial ecosystems, investigators have found that fungi and bacteria are actually driving plant productivity. In other words, ecologists had omitted the most important players in their models of ecosystem function. A potent mechanism at work here is the role of fungi in plant disease. As plant diversity decreases, the impact of a single pathogen becomes amplified. This is obvious in the case of monoculture agriculture: if a wheat field is attacked by a rust, crop productivity falls and there are no other plants to take up the slack. The same sort of thing happens in natural ecosystems. The impact of a single pathogenic fungus tends to be muted if plant diversity is high. This is a matter of common sense.

Interactions between plants and microbes go well beyond the effects of pathogens, of course, and studies show that harmless soil microbes impact plant productivity through their influence upon nutrient availability. Most plants do not thrive in microbe-free soils, and the usual relationship between plant diversity and productivity collapses without bacteria. Ecosystems, like individual animals, don’t work very well without microbes.

All biologists have known for decades, if they thought about it, that microbes are more important than frogs in maintaining a biosphere capable of supporting humans. Tom Curtis championed the microbiological view of ecology with the following provocation:

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-oxidisers [bacteria], it would be another matter. It could be happening now and we wouldn’t even know.

Watching a breaching humpback whale off Cape Cod and hearing the massive exhalation through its paired blow holes, it seems clear that the mammal is running the show. A microscope and some imagination are required to relegate the whale to the background and absorb the fact of the microbial hegemony in the grey Atlantic water and everywhere else. The act of putting a drop of fluid on a microscope slide and viewing it at up to 1,000 times its actual size can be an awe-inspiring experience, no less a thrill than looking at the night sky with a telescope or binoculars. Microscopes and telescopes make the invisible visible: the night sky dotted with a few weak stars becomes an endless shower of light; a cloudy drop of pond water is filled with spinning, whirling, and gliding cells.

By adding microbes to the public discourse we may get closer to comprehending the real workings of the biosphere and the growing threat to their perpetuation. Interest and indifference to conserving different species shows an extraordinary bias in favour of animals with juvenile facial features, ‘warm’ colouration, ‘endearing’ behaviour (fur helps too), and other characteristics that appeal to our innate and cultural preferences. The level of discrimination is surprising. Lion cubs have almost universal appeal, and it must take a lifetime of horrors to numb someone to the charms of a baby orangutan. The charismatic megafauna are very distracting, and the popularisation of microbial beauty will require a shift in thinking, a subtlety of news coverage, a new genre of wildlife documentary. The ethical responsibility lies with the nations that are engaged in modern biology.

We have come a long way, and been humbled greatly, since Pliny the Elder embarked upon his hopeless plan to record “all the contents of the entire world” in his encyclopedic Naturalis Historia. Modern research on microbial diversity has shifted from the microscope to the automated sequencer. This has revealed an astonishing breadth to the variations in the smallest forms of life. Two thousand years after Pliny, however, we are little closer to completing his catalogue. Harvard ethologist E.O. Wilson recommended another shot at this task through his Encyclopedia of Life project. The quixotic nature of the endeavour was obvious to anyone who thought about it for a few minutes, and the stocktaking has failed to overcome Wilson’s preoccupation with animals. Interest in this futile task continues, with calls from other prominent scientists for naming species “before they go extinct.” A cheerful projection suggests that a catalogue of five million or so species could be completed within 50 years at a cost of around US$1 billion per year. The authors of this estimate argue that by naming things we might be in a better position to curb their annihilation. Is this sensible?

Name recognition isn’t a big problem for tigers and rhinoceros. More logical justifications for this taxonomic marathon speak to the fundamental importance of identifying something as a species to enable the proper exploration of biodiversity, and another stimulus is that the inventory would help determine rates of extinction. There is a strain of desperation here. Today’s biologists working on this encyclopedia would become co-authors of a holy book of sorts, a Testament of Ignominy against which future generations could gauge how much damage we did.

An obvious shortfall of this proposal, as its proponents would agree, is that it wouldn’t tell us anything about microorganisms. And that is a tremendous problem and one of the stumbling blocks to accepting that a 50-year taxonomic exercise is worth funding. Biologists, as a community, are still finding it difficult to emerge from the stamp-collecting stage of our science. Whether we are talking about molecular methods or dried sheets in herbaria and drawers filled with disembowelled birds, the importance of the taxonomic exercise deserves some objective analysis. Physics did not stop after Newton; why did so much of biology conclude ‘Mission Accomplished’ after Darwin?

If extinction is the thing we are trying to forestall, we would be better placed in trying to save habitats. The inhabitants of threatened forests would tend to come along automatically, subject to the usual problems with poaching in the remaining wildish places. Because animals and their onboard microbes live in specific habitats, and the habitat is defined, to a large degree, by its plants and the soil microbiome, saving a forest can conserve a lot of things without our ever knowing that they are there.

There is some merit in thinking about ‘The Selfish Bacterium’ as an analogue to Richard Dawkins’ popularisation of the gene as the element of continuity throughout the history of life.”

Another challenge for biologists trying to understand the activities of the smallest organisms is that most of us are unaccustomed to thinking about the spatial scale of the environment that matters to a single cell. Each of the planktonic bacteria in my garden pond has a unique life experience shaped by fluctuations in the availability of dissolved ions, changes in temperature and light intensity, contact with other bacteria, and attack by viruses. Gene expression inside the tiny cells is adjusted to maintain energy production and maximise the prospects for cell division. Motile cells with spinning flagella navigate the pond water, responding to gradients in dissolved oxygen and organic nutrients as well as local clouds of metabolites secreted by other organisms. Faeces puffed from fish add pulses of organic matter to the pond and drops of tree sap plummet through the water column leaving tails of syrup like tiny comets. The pond is a mosaic of microbes and their food. Bacteria lacking flagellar motors are moved by ripples from the pond pump and the flicking of fish tails; convection currents circulate the water too, bringing colder water from the bottom toward the surface warmed by sunbeams; a rain shower cools and mixes the surface water and the bellyflop of a frog is the microbial equivalent of an asteroid strike.

There is some merit in thinking about ‘The Selfish Bacterium’ as an analogue to Richard Dawkins’ popularisation of the gene as the element of continuity throughout the history of life. Humans, for familiar example, can be regarded as temporary conduits for primate genes, as carriers of an immense repository of prokaryote and viral instructions, or as shills for the transportation and replication of bacterial mitochondria. All of these representations have some scientific validity. None of them affect the preoccupation of the individual with everyday concerns – familial, financial, and so on.

For some people the scientific deconstruction of the body has a profound effect upon tolerance for the vagaries of religious doctrine. Deep engagement in the principles of Darwinian evolution has shaken, if not abolished, the faith of many people in supernatural ideas about the special place of Homo sapiens in a grand scheme. Even then, the agnostic biologist spends more of the time worrying about her daughter’s dental appointment than she does revelling in the fact that everyone in her family is energised by bacterial proteins in the inner membranes of their mitochondria.

Knowledge of the gut microbiome changes the balance a little. Our highly bacterial nature seems significant to me in an emotional sense. I’m captivated by the revelation that my breakfast feeds the 100 trillion bacteria and archaea in my colon, and that they feed me with short-chain fatty acids. I’m thrilled by the fact that I am farmed by my microbes as much as I cultivate them, that bacteria modulate my physical and mental wellbeing, and that my microbes are programmed to eat me from the inside out as soon as my heart stops delivering oxygenated blood to my gut. My bacteria will die too, but only following a very fatty last supper. It is tempting to say that the gut microbiome lives and dies with us, but this distinction between organisms is inadequate: our lives are inseparable from the get-go. We carry the microbes around and feed them; they deliver the power that allows us to do so. Viewed with some philosophical introspection, microbial biology should stimulate a feeling of uneasiness about the meaning of our species and the importance of the individual. But there is boundless opportunity to feel elevated by this science. There are worse fates than to be our kind of farmed animal.

Adapted from The Amoeba in the Room: Lives of the Microbes, published by Oxford University Press.

 

Nicholas_P_Money_224Nicholas P. Money is Professor of Botany and Western Program Director at Miami University in Oxford, Ohio. His previous books include Mr Bloomfield’s Orchard: The Mysterious World of Mushrooms, Molds and Mycologists and Mushroom.
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