Liaisons of Life

by Tom Wakeford John Wiley & Sons, Inc. 2001

Excerpt from Introduction:

In The Death of Nature, Carolyn Merchant vividly describes how the scientific revolution of the 17th & 18th centuries wrote nature and women out of the process of acquisition of knowledge. Here I describe how microscopic nature was written out during the 19th century - laying the foundations for our current obsession with genes as the only biological/evolutionary force.

Historians suggest that a key factor preventing scientists from exposing these associations between plants, animals, fungi and microbes was the lack of the appropriate laboratory technology to carry out critical experiments. ‘Good scientists’, said Nobel prize-winning immunologist Peter Medawar, ‘study the most important problems they think they can solve’. ‘It is after all’, he concluded, ‘their professional business to solve problems not merely grapple with them. If politics is the art of the possible, research is surely the art of the soluble. Both are immensely practical-minded affairs’. Examining how microbes form liaisons with animals or plants is a quantum leap in experimental complexity from looking at how either of the two groups associate with each other.

Apart from being so very small and difficult to study, the second misfortune to befall microbes was the grim circumstance in which bacteria first received notoriety. Fame was thrust upon them during research not into flavours of cheese or the bouquet of wines, in which they are the crucial ingredients, nor into agriculture, where they ensure the fertility of crops. Instead they were immortalised by medical research, where their presence in the blood was seen as a sure sign of disease. Finding non-pathological microbes rather complex and confusing, microbiologists followed the path of least resistance, and greatest public fear, and studied those that appeared to be deadly pathogens.

Nineteenth-century French researcher Louis Pasteur single-handedly spawned the anti-bacterial age. His cult of cleanliness prevented us seeing our microbial associates as anything other than invisible assassins. Though some of his first and most notable achievements were to improve management of the highly productive bugs that were the active ingredient of the sugar distilling and wine industries, Pasteur is most famous for renaming bacteria ‘germs’. Becoming increasingly shrill as his fame increased, he advised that these enemies of the people should be tracked down and destroyed.

Pasteur was undoubtedly a pioneer in tackling the bacteria that cause disease. In 1881 he devised vaccine for anthrax, a fatal disease that threatened French sheep farmers. In 1885 he claimed to have invented a vaccine for rabies, though historians have recently questioned his account. His innovative techniques quickly lead to the development of vaccines for TB, cholera and the plague. His ‘pasteurisation’ process for cleansing milk of tuberculosis bacteria continues to this day. Yet Pasteur's championing of the view that disease was solely due to bacteria and bore little relation to the malnutrition of the victim, was controversial. Many doctors of the time argued that it was far more important to improve the nutrition and living conditions of the poor than to identify the bacteria that finally infected and killed them.

An intensely political animal, Pasteur once stood as a candidate for the French Senate. In his characterisation of bacteria, he adopted terminology that could not endear his ideas to his fellow conservatives. He shared their terror of the mob ? that mass of faceless peasantry, whom he charged with murdering his King during the previous century’s Revolution and instigating the terror against the aristocracy. Writer and historian David Bodanis has demonstrated how the language Pasteur used against these masses was almost exactly the same as that which he developed to characterise bacteria:

Let the mob take Paris and without the King or Emperor to shore us up we would dissolve into aimless bodies no different from the mob; let the bacterial mob take our physical body and we would decay into a putrefying bacterial mass no different from the attackers. If unpleasant entities such as the people or bacteria had to exist, then they must be kept firmly in their place. The people, especially the workers, were safe only if kept in passive Catholic trade unions, or state-run clubs, or other trustworthy bureaucratic bonds. The bacteria, in all their unpleasant and quick-to-grow varieties, were safe only if restricted to one slot in the Great Chain of Being, that of the decomposer of dead bodies, destroying order only after all life in it had naturally gone, and returning its atoms to the soil for re-birth. Outside of that, though, and they were terrible.

Pasteur’s students testified how he could sow, cultivate and domesticate his microbes so that the invisible became tangible to the ordinary onlooker. He was alone in being able to pacify the enemy within. Gerald Geison, historian at Princeton University, calls him the ‘artist of the invisible world’. But he was also an army general in a war to impose his new scientific theories in which words were used as battle cries. His legacy as a scientific genius, and would-be microbe-killer, cast a shadow over microbiology for the next seventy years. To be numbered among his followers, was to see human health as a theatre of war, with bacteria as the swarm of invisible enemies to be destroyed.

By the late 1890s the imagery of a loathsome bacterial mob had become such a part of everyday life, that it became one of the most common metaphors used by early British war correspondents. As General Kitchener’s army descended on Egypt, the Daily Mail’s reporter described the enemy as ‘swarming up the hill…like a torrent of death’. During the First World War, sections of the British Press began to called the Germans ‘GermHuns’, who, said the New Statesman, must be stopped as if they were ‘an epidemic of scarlet fever’. The idea of surrounding an enemy army so completely that none of them can escape is still referred to with the bacterially inspired French phrase ‘cordon sanitaire’.

Epidemics of disease afflicted those successive waves of European immigrants who, often malnourished, arrived in the United States, first from Ireland, Germany, and Scandinavia - in the nineteenth century, then Italy, Eastern Europe and elsewhere continuing well into the twentieth century. Little surprise, then, that among the most enthusiastic followers of Pasteur's germ theory of disease were doctors in the cities of the US East Coast. In the 1920s and 30s this enthusiasm reached fever pitch. At the same time as Stalin was purging his country of potential intellectual 'enemies within', America suffered a collective wave of anti-microbial paranoia, fed by the newspapers and books of the day. Most famous of these was The Microbe Hunters by Paul de Kruif, published in 1926. He described bacteria as 'invisible assassins' who, like the Chicago gangsters of the time, should be shot 'with magic bullets'.

De Kruif's book is a brilliant crime novel, in which scientists are cast as the defenders of private property, while bacteria play the part of thieves and murderers. ‘These wretched microbes’, he wrote, ‘kill millions of human beings mysteriously and silently’. He concluded that these germs were ‘more efficient murderers than the guillotine or the cannon of Waterloo’. His words influenced successive generations of industrial civilisation, yet we now know that disease-causing bugs make up only a tiny fraction of the total diversity of microbes.

A randomly chosen bacterium is far more likely to be digesting your domestic sewage or supplying oxygen for you to breathe than it is to be making you ill. The vast majority of bacteria live harmlessly and unobtrusively on the surface of our seas and in our gardens, quietly undertaking biological processes crucial to every ecosystem. Many species are essential to the production and digestion of almost all of the kinds of food that we eat, the recycling of our wastes, and the fertility of our soils. Some bacteria do kill, though ironically they often do so by producing toxins, which are a sign that they themselves are under stress. Metaphors that cast all bacteria as germs have obscured our biological understanding for too long. In reality, pathogenic microbes are the exception, not the rule.

By the time I took my final exams, the world of conventional ‘big biology’ seemed a world away from all this. Virtually everything seemed to be turned on its head by taking a microbe-eyed view of life. Microbes are not the deadly killers that must be cleaned from every nook and cranny at the first opportunity, but have rather been crucial innovators in the past four billion years of evolution. It came as no surprise to learn that the eminent Harvard University ant-watcher and biologist E.O.Wilson, when asked what he would do if he were to have his time again, replied that he would like to have been a microbial ecologist. Because of the minute scale and speed of their activities, the bug’s life - spent on our teeth, in our guts, or in our oceans is only just beginning to be uncovered.

The diversity of microbes is even greater than that of insects. Vigdis Torsvik, a bacteriologist at the University of Oslo, Norway, has found that an average teaspoon-full of soil contains around ten thousand different genetic types of bacteria. If you extracted all the bacteria from two acres of farmland, their total weight would be greater than that of one hundred sheep. Another area in which microbes may outdo the animal kingdom is in their extraordinary sex lives.

Unlike other aspects of their lifestyle, the sexual antics of bacteria have been well researched over the past fifty years, mainly because of their relevance to treating human disease. If it were not for sex, the life of a bacterium would seem rather uniform. Animal or plant cells can change into a million different cell types - a petal, an eye, or a skin cell. In contrast, a bacterium stays the same size, in the same rod shape, almost all its life. While any given mammal cell is only likely to express five per cent of its genes during its life span, a bacterium uses most of its genes, most of the time. Because they reproduce so frequently and at such speed, bacteria that carry too many genes waste energy copying them every time they reproduce. They would be quickly overtaken by other less encumbered strains. Microbial geneticists have found that bacteria undergo a kind of gene-injecting sex that occurs quite independently of the bacterium's reproductive cycle, allowing them to import new genes throughout their lifetime without waiting to reproduce.

Popular accounts of the natural world have found the bacterial scale of life difficult to depict. Yet by retreating into a mere focus on fierce or furry creatures they risk distorting our understanding of ourselves and our place in biology. By concentrating on mammals, they re-enforce the suspect notion of evolution as progress, inexorably moving towards its summit - humanity. The suggestion that bacteria are primitive beings that long ago passed the torch of evolutionary innovation on to large organisms is misguided. Bacteria are the eternal innovators in the history of life. Biology without bacteria is as incomplete as physics that ignores atoms and molecules.

As our continual medical battle with disease testifies, bacteria have shown themselves to be our equals. They not only invented most biological processes ? everything from sex and light reception to breathing and movement ? but almost every biologically-generated chemical on Earth. Bacteria also spearheaded the evolution of the other four kingdoms of life. Every time we make use of microbes, in making yoghurt or cleaning oil slicks, we are drawing on four billion years of incomparably sophisticated yet sub-visible innovation. It is no surprise that out of the three diseases virtually defeated by modern medicine ? smallpox, polio and measles - none are microbial (they are viral), whereas of the three biggest current killers ? malaria, TB and HIV - two are microbes.

Microbes and their liaisons are fundamental to the origin, evolution, and current function of every creature we encounter, from the hornwort to the hippo. Even our understanding of ourselves is greatly advanced by taking a new microbe-eyed view. Today it makes no sense to study evolution or ecosystems, be it in our garden soil or at the bottom of the Atlantic Ocean, without recognising the keystone activities of our microscopic cousins. Indeed, three of the most important breakthroughs of the past half century - symbiogenesis theory, microbe-mediated immunity and the Gaia hypothesis - have all challenged traditional biological theories by uncovering the hidden powers of the microbial realm.

Our new-found knowledge of microbes, and the intimate liaisons in which they become involved, is fuelling a transformation in the scientific world-view. The chapters that follow chart the development an integrative history of life on earth from this new perspective, which has even reached Hollywood. Amidst scenes of inter-galactic warfare, the latest Star Wars movie reveals the origin of the Jedi’s mysterious ‘Force’ as being the symbiotic life forms inside their cells.

In biology, symbiosis is the term used to describe long-term intimate associations between different organisms, usually involving a microbe. Such liaisons, be they between animal and alga, or zooplankton and zebrafish, are fundamental to the development of every living system. Drawing on new evidence from creatures found in settings as diverse as underwater volcanoes, termite mounds and the gaps between our teeth, this book argues that staying alive is as much about bonding with your neighbours as it is about growing and reproducing.

Despite having been first proposed more than a hundred years ago, the idea that liaisons with microbes are a primary means by which evolutionary innovation has taken place has taken over a century to reach centre-stage. Each chapter explores the mixture of personality politics, technological backwardness and blind ignorance the led the revolutionary ideas of a handful of pioneers to be condemned as heresies, only to be celebrated today as some of the greatest breakthroughs in the history of science.

In 1896, Beatrix Potter came face to face with the first barrier for the symbiosis pioneers - ignorant prejudice. The soon-to-be-famous children’s illustrator was hounded out of biology by the closed ranks and narrow minds of London’s top scientific institutes. Their members refused to accept Beatrix’s evidence that the curious living encrustations, known as lichens, on tree-trunks, seashores and walls, were made up of not one but two organisms in intimate liaison. Yet her insight was more far reaching than either she or contemporaries could ever have dreamt.

Not only lichens, but also almost every tree, bush and grass on Earth leads a double life ? married to a fungus. While orchids and oak trees appear to be individuals, in reality they live in an inextricably interwoven liaison with a world-wide web of underground fungal foragers. A hundred years after the stifling of Beatrix’s search for natural truths and her final retreat into voluntary exile, we can now celebrate her revolutionary new view of life. Inter-connectivity can be a strength rather than merely a source of potential conflict - a vital resource rather than a drain.

Even after the great man’s death, Pasteur’s influence not only pervaded the medical laboratories of Europe and America, but even the study of the evolution of marine life. Many of the most spectacular examples of animal symbioses are buried deep in the ocean abyss, but much of the work of the early investigators into this astonishing realm was crushed by Pasteur’s supporters. In the weird world of the sea bed, biologists have now discovered a spectrum of luminous animals. New genetic techniques have revealed that their glow is a gift from their bacterial associates. While deep-sea fish have their own microbial searchlights for hunting in the blackness, octopuses and squid use these glowing symbionts as a disguise from predators, or to chat up the opposite sex.

In the case of insects, the latest molecular tools, such as DNA fingerprinting and luminescent gene-markers, have exposed the pervasive influence of bacteria on beetles, butterflies and blowflies. They have power over wide ranging aspects of an insect’s life including sex-determination, digestion and nest-construction. Genetic analyses have also revealed the extraordinary gardening exploits of the ants. By building their own self-fertilised fungal farms, cultivating a continual harvest, and swapping favourite crop varieties with their neighbours, ants have achieved a sophistication of microbial liaison that may have lessons for the way we feed ourselves. Some researchers predict that one day symbiotic bacteria may even be shown to provide the mechanism behind the extraordinary diversity of insect life on Earth.

Historians of science have puzzled over why these fundamental insights took so long to receive recognition. Primitive analytic tools, Pasteurian paranoia, and intellectual inertia are part of the explanation. But, tragically, the study of symbiosis also fell foul of global politics. World wars, nationalism, anti-communism ? these and other global tensions have dogged the understanding of the liaisons of life for more than a century. Symbiosis was invented as a purely scientific term, but it was fatally bracketed in the minds of its enemies with dangerous political movements. Nor did it help that the pioneers in this field were largely from non-English-speaking countries such as France, Germany and pre-revolutionary Russia. In the wake of the carnage of the First World War and the new threat from the Soviet Union, symbiosis was condemned by mainstream science as a political subversion that could neither provide explanations for humanity’s apparent lust for conflict, nor the evolutionary patterns of life. The study of symbiosis became an international pariah, subject to almost Macarthyite witch-hunts among professional scientists and tacit textbook censorship.

In the 1990s, symbiology at last escaped across biology’s own Berlin Wall. Those who had championed the significance of symbiosis for decades finally saw their ideas triumph, not just because new genetic techniques strongly supported their theories, but also because their fellow scientists became more open to a symbiotic perspective. The latest research poses exciting challenges to received scientific wisdom. Far from all organisms being in constant competition, many seem to have bonded to such an extent that it is no longer possible to tell where one ends and another begins. In changeable environments such as the forest floor, it seems that microbes provide resources to its extended family according to the recipient’s needs.

The sudden transformation in symbiotic understanding during the past few years heralds the final hurdle for life’s liaisons - the challenge they pose to traditional evolutionary theory. Brought up on the orthodox story of life evolving via chance mutations and competitive struggles, biologists struggled to comprehend a world of microbial mergers and emergent wholes. New-found knowledge of widespread intimate association in nature is now adding a new dialect to the language of Darwinism.

A model of life that recognises the key role of our associates offers a new scientific toolkit for the twenty-first century. It helps us resolve the tensions between the holistic and reductionist views of life, the role of nature and nurture in development, and the relative importance of the individual and its community.

In both biological science and in our everyday life, we have the beginnings of a new relationship with our planet based on a more complete understanding of wild and domesticated nature. This new perspective recognises the centrality of microbes in all living systems, our inescapable connectivity with them, and the importance of maintaining liaisons with our neighbours and associates. Having reclaimed a radically new way of looking at life after a century during which it remained at the margins of science, Liaisons of Life suggests how we can build new alliances for the future.

Excerpt from New Gardeners of Eden

In the final chapter I summarise a lot of the evidence presented in previous chapters and outline a new perspective on evolution that might be dubbed ecological Darwinism.

The final section looks at the dynamism of biological systems, the origin of some GM crops and the urgent need for science to re-focus.

So the first two key tenets of ecological Darwinism seem robust: that microbes are one of the most, if not the most, important innovative factors in evolution; and the interdependence among organisms is at least as important as competition between them. The third, which suggests that intimate associations such as symbioses are inherently dynamic, holds perhaps the most radical implications for evolutionary theory. Today’s mutualist can become tomorrow’s parasite depending not on what genes it contains, but on what fortunes fluctuation in its environment may bring. A fungal mycorrhiza can be a net drain or a net contributor to a plant’s nutrition depending on a variety of factors such as soil type, season, and even the weather. The widespread bacterial symbiont of insects, Wolbachia, brings advantages but also fatalities among a wide variety of insect species. Some of the bug’s effects differ depending on what point the insects have reached in their life cycle.

In 1904, the chestnut blight fungus was imported into the US and started to infect chestnut trees, apparently causing them to die. Yet these trees are still alive today. Instead of dying they have re-grown as bushes of seven or eight feet in height. If any shoots get above this height, the fungus develops and they die back. The bush now occupies a new niche in American forests, and the fungus even seems to give the tree some protection against viruses. So is the fungus a parasite or a mutualist?

Biological liaisons are inherently dynamic phenomena. Rather than discrete categories, the terms mutualist, parasite and pathogen are better seen as fuzzy points on a continuum, along the length of which an association between two organisms may fluctuate. For many associations, the point they occupy on this continuum is as difficult to assess as it is to say who gains more on average in a marriage between two human partners. Describing symbiosis in their 1930 textbook, H.G. Wells and Julian Huxley showed that they understood this variability well:

As in the more plastic of human relationships, casual association may pass over into mutually helpful partnership, or transform partnership into parasitism. How difficult it may be to distinguish between service and slavery.

,Biologists have even managed to engineer a move from pathology to mutualism in an association between a watermelon and a fungus. Two plant geneticists, Stanley Freeman and Rusty Rodriguez, of the University of California, Riverside transformed a fungus that caused disease in watermelons into an internal associate that actually seemed to enhance the melon’s growth. They achieved this turn around by changing a single gene

The idea of a dynamic continuum of associations also applies to how intimate they are. At one end of the continuum is an association such as the mitochondrion or chloroplast where a bacterium has become so integrated into the metabolism of another cell that it has undergone a permanent merger, losing its independent existence and many of its genes. These kinds of intracellular symbioses, where the descendants of bacteria become permanent inhabitants of the cell, are inherited through the sex cells and are automatically present in every cell of the offspring. At the other extreme come the termites and leaf cutter ants. Their cultivated fungi farms are passed on to future generations of termites and ants, but only by a process of re-infection by the young picking up the fungus directly from the faeces of adults. It is a cyclic rather than a permanent association. By comparison, the legume-rhizobia symbiosis is a mixture of the two extremes: the relationship has to be reformed yet again every summer as pea and bean seeds germinate and develop roots.

The ideas and theories described in this book would be of limited interest if they were only relevant to purely scientific squabbles about how life began, innovated or evolved. Yet an understanding of the liaisons of life can do far more. An ecological Darwinist approach has vital implications for the way biological theories are applied in the real world, whether through medical, agricultural or other biotechnologies. An evolutionary perspective not only points to possible solutions to our current dilemmas, but also helps explain how we went wrong in the past. Our cultivation of legumes, the plant family that includes many of the world’s staple food crops, provides a particularly striking example of how scientists have neglected the key features of intimate biological associations.

In the mid-1980s rhizobia was one of the most highly researched non-pathogenic microbes on Earth. Using recombinant DNA and other genetic engineering techniques, geneticists promised strains of the bacteria that would out-compete any indigenous bacterium and double farmers' crop yields. After ten years of research not a single genetically engineered rhizobial product had been successfully marketed and all the biotech companies had withdrawn from this area of research. Despite thousands of field tests aimed at determining the best rhizobia strain for a particular crop, the world-wide market for inoculants remains insignificant, because farmers find that their yields do not improve. Scientists discern a small improvement in yield using inoculations of the engineered strain in a laboratory greenhouse, but in field conditions the beneficial effect disappears. What went wrong? One factor seems to be that legumes prefer bonding with rhizobia that they have domesticated themselves rather than ones that scientists have sought to genetically engineer for them.

There is another evolutionary reason why genetically engineered symbiotic bacteria fail. Unless a permanent merger has been formed, such as a mitochondrion or chloroplast, it would be in no organisms' evolutionary advantage to commit itself to just one breed of domesticated associate. So many organisms put their symbionts out to tender with every new generation rather than rely on a monoculture of any single variety. The algae-juggling corals and fungi-swapping ant and termite colonies are illustrations of this principle. Similarly, pre-industrial agriculturists, modern organic systems, and many of today's Third World farmers, try to keep a range of varieties of any given domesticated crops on their farms, in case environmental conditions demand one rather than the other. Another reason monocultures are rare in nature is because they make life easy for pests. Genetic uniformity in an agricultural system is analogous to providing every house in the neighbourhood with the same lock on their front door. If burglars can get into one home, they can get into any of them.

In the rush to identify genes for drought-resistance and salinity-tolerance, commercial biotechnologists may ignore the microbial liaisons that already allow many plant species and traditional crop varieties to survive such harsh conditions. For centuries a wide range of crops have been given this resistance by naturally occurring fungal symbionts. These integral associations are the first casualties when genetically engineered varieties, and their attendant fertilisers, herbicides and pesticides, replace the complex cultivated biodiversity with their lifeless uniformity. As Kansas farmer and philosopher Wendell Berry has said, these people do not know what they are doing ‘because they have no idea what they are undoing’. The fields where the companies grow their crops are so permeated with chemicals and lacking in natural compost that the indigenous fungi and other microbes, of which the companies scientists have such little understanding, find it hard to survive.

At the same time as our soils are threatened by the further industrialisation of agriculture, there are encouraging signs of a growing grass-roots movement that emphasises the need for a reciprocal relationship between humanity and our land. All over the industrialised world, the demand for farm products that respect the need for the self-regenerative dimensions of a cultivated system is growing. Organic or ‘natural systems’ agriculture draws on the wisdom of farmers who, over thousands of years, learned to work within their environmental constraints, and constantly strove to breed a diverse range of plants and animals that met their need for continuing food supplies despite variations in climate, pests, and soil conditions.

Organic methods arise from a complex ecological understanding of, combined with sympathy for, the land and organisms with which they work. A research team led by David Pimentel at Cornell University has demonstrated that well managed organic systems can produce yields just as high as chemical-based agriculture. During the Second World War, Britain produced a quarter of its food supply from millions of its citizens working on their allotments, with virtually no use of artificial chemicals.

In some countries, organic methods are rapidly returning to farms and becoming the norm once again. At a recent exhibition held by an association of agrochemical companies in Lithuania, the country’s Deputy Prime Minister received them with the following greeting: ‘You are very welcome to come and meet us here in Lithuania, but your style of farming has no future in this country.’ Fields in the former Yugoslavia, in which landmines kept farmers from growing fertiliser- and pesticide-sprayed crops for several years, now gives them the perfect ecological conditions to return to the organic methods of their pre-Soviet ancestors. Farmers across Eastern Europe are resisting the overtures from chemical companies and are instead using the organic techniques passed down from a previous more enlightened era.

In India, one of the prime targets for the trans-national biotechnology companies, my visits to villages in some of the poorest regions convinced me that genetically engineered crops come very low on the list of priorities for increasing the amount of food that is produced by the country’s marginal farmers. When asked what would agricultural improvements their livelihoods most significantly, most poor farmers ask for easier access to water, and farm-yard manure to restore fertility to their land, which has been robbed of organic matter by decades of use of government-promoted chemical fertilisers.

After two hundred years, in which we have been almost blind to the extent that our activities are ultimately constrained by our ecological relations, humanity may, like Voltaire's Candide, at last becoming conscious of its green-fingered essence. An approach based on nurturing our associates is bringing about a revolution, not only in how we produce our food, but in the way we think what life is, and how we evolved.

Russian émigré and father of the modern evolutionary synthesis Theodor Dozhansky famously said that ‘nothing in biology makes sense except in the light of evolution’. If we accept an ecological Darwinist approach, nothing in the living world will look quite the same again. Perhaps its most urgent practical message is that we need to become more actively aware of the full extent to which our futures, like those of all organisms, are ecologically bound up with those of a larger biological whole. Whether by destroying our soils with industrial agriculture or burning up the atmosphere with our cars, we risk disturbing this living global system beyond its capacity to support us. Our planet could move to a state that is no longer as hospitable. Perhaps we are already reaching that point. As products of four billion years of evolution by association, we need to rapidly learn to be wise gardeners of our Eden, or we risk having the worst of all possible worlds.

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