Invisible world, invisible saviors: The secret to overcoming the threat of extinction

If we want to avoid the worst ecological catastrophes, we're going to have to begin thinking small. Very small

Published March 30, 2014 2:00PM (EDT)

The bacterium, Enterococcus faecalis, which lives in the human gut.  (AP/Agriculture Department)
The bacterium, Enterococcus faecalis, which lives in the human gut. (AP/Agriculture Department)

Excerpted from “The Amoeba in the Room: Lives of the Microbes”

History, according to the heartfelt judgment of a young scholar in Alan Bennet’s marvelous 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 neighbors, 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. Until the seventeenth century, the obvious impediment was our blindness to things smaller than fleas. The slight magnification of nature by Galileo’s friends at the Accademia dei Lincei—no more than a well-made hand lens can show us today—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.

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. Investigators identified a number of variables that influenced species richness, including climate, the heterogeneity of habitats within the ecosystem, and the abundance of solar radiation. Rain forests support lots of species because their climate is relatively uniform throughout the year, the trees and shrubs create an abundance of distinct habitats, and the sun shines year round. The stability of the ecosystem is another significant consideration. Some tropical forests are so old that evolution has had time to birth many of their younger species.

Contemporary ecologists continue to study these questions, but they recognize now that species richness is only one of multiple measures of biodiversity. Defining the spatial scale of the analysis is important. Some scientists are interested in patterns of diversity within a particular ecosystem, comparing the tree canopy with the shrub layer of a forest, others are concerned with a finer scale, studying differences between neighboring patches in grasslands.

It is evident that ecosystems which support greater numbers of species are also the most productive. The mechanistic link between diversity and productivity is another of the key questions in ecology. The most compelling explanation is that different species make use of different sets of resources so that an assortment of plants has a harmonizing effect, maximizing photosynthesis in a given area of grassland or forest. This is called niche complementarity. The concept is complicated by the realization that the range of plant types, rather than the number of species, is a stronger determinant of stability and productivity than species richness alone. Sedges, for example, are better at growing in waterlogged soils than grasses, which means that a mixture of sedges and grasses may be more productive than the richest assortment of grasses.

For a long time, 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 specialized endeavor.

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. It is no longer permissible for a plant ecologist to ignore soil microorganisms: there is little likelihood of receiving funding for experiments on an invasive plant species that makes no effort to examine the diversity of associated mycorrhizal fungi. 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. One approach to studying the details of these symbioses is to control them by growing the plants in sterile greenhouse facilities in containers, or microcosms, filled with soil mixtures inoculated with particular fungi and bacteria. Microcosm studies are unambiguous in demonstrating the reliance of the majority of plant species on fungi that establish mycorrhizae. Complementary macrocosm experiments, in which field plots are inoculated with fungi, show that the number of plant species tracks the number of fungi. Finally, most plants do not thrive in microbe-free soils, and the usual relationship between plant diversity and productivity collapses without bacteria. The outcomes of these experiments are reminiscent of the observed debilitation of germ-free, or gnotobiotic, mice. Ecosystems, like individual animals, don’t work very well without microbes.

Microbes are also imposing themselves upon more specialized fields of ecology. Restoration ecology concerns the rehabilitation of damaged ecosystems and contaminated soils. Plants were the sole focus of this inquiry a decade or so ago. Today, investigations on mycorrhizal fungi in these habitats and their interactions with plants are de rigueur. Conservation biology has lagged behind restoration ecology in this respect and remains fixated upon macrobiology. When microorganisms are included in conservation studies they appear only as disease agents of larger, more interesting species. The fungal pathogen of amphibians has made it to primetime in the major journals concerned with conservation, and microbial pathogens of trees wax and wane according to the current newsworthy epidemic—Dutch elm disease, sudden oak death, ash dieback. The lack of interest in the rest of the news about microorganisms, which is almost the entire story, is almost comedic.

Some of this neglectfulness can be pardoned by the fact that until the advent of metagenomic technologies microbial ecologists had too little to contribute to the topic of conservation. There wasn’t enough information on the bacteria in soils to say anything meaningful about their importance in plant diversity. Nevertheless, 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-oxidizers, it would be another matter. It could be happening now and we wouldn’t even know.

Whales, as I explained earlier, have little effect on nutrient cycling compared with the energy fluxes through marine microbes. This fact has no bearing upon the human relationship with whales, or the importance of whales to themselves and to the organisms that they consume and those that consume them. 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 is required to relegate the whale to the background and absorb the fact of the microbial hegemony in the gray Atlantic water and everywhere else.

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 favor of animals with juvenile facial features, “warm” coloration, “endearing” behavior (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. But we make subconscious rankings of animals of every stripe. Among penguins, for example, we prefer species with bright yellow or red feathers. The charismatic megafauna are very distracting, and the popularization 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.

I've previously mentioned the quixotic proposal to catalog every species championed by the Harvard biologist E. O. Wilson. 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 catalog of five million or so species could be completed within 50 years at a cost of around US$1 billion per year. This is less than 2 percent of the annual federal investment in scientific research in the United States. 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 disemboweled 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.

Greater appreciation of the microbial isn’t guaranteed to change the study of biology. The application of metagenomics has already resulted in a groundshift in the science, but there are a lot of uncertainties about the most fruitful ways to proceed. The sheer size of microbial populations suggests that current sampling methods may be inadequate to the task of assessing genetic diversity. A DNA library of 1,000 clones sounds impressive, but if this was amplified from the community of more than one trillion microbes in the nutrient-rich water of my small pond we would have sampled fewer than one in one billion of its cells. Some comfort is found in the annual increase in sequencing speeds and decrease in costs per sequence. The most ambitious experiments on the gut microbiome have analyzed 10,000 or more clones from single samples, and yet the potential shortcomings of the molecular exploration remain. The diversity of a microbial community increases with the detail and depth of the analysis; the more we probe, the more we see. One trillion is an awful lot of individual cells.

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 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 maximize 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 eukaryotes. Feces 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 belly flop of a frog is the microbial equivalent of an asteroid strike.

Besides the planktonic bacteria, prokaryotes swarm in the silt and over the plastic surface of the pond liner. Bacteria coat algal filaments and the leaves of plants dangling in the pond. Other microbes fill the guts of the fish, frogs, and invertebrates. Every community displays a different version of behavioral complexity. Quorum sensing allows a population of cells to gauge its density and coordinate gene expression. Bacteria secrete signal molecules called autoinducers that diffuse throughout the colony, and the concentration of these chemicals serves as an accurate proxy for the number of collaborating cells. When the level of this compound reaches a particular threshold it triggers community-building activities like the dense packing and adhesion of cells to create a protective biofilm. In other conditions, quorum sensing activates the invasive growth of pathogens, spore formation, and bioluminescence.

The range of activities of individual microorganisms added to the genetic and physiological diversity of bacteria complicates the goal of developing a holistic description of any ecosystem. Macrobiology is knotty enough on its own, but the introduction of the microscopic can drive models of ecosystem dynamics to spectacular levels of incomprehensibility without enhancing their predictive power. My book, "The Amoeba in the Room," began with a quest to comprehend the diversity of organisms in my pond. This relied, for the most part, upon the use of the microscope. The analysis of the sea, soil, air, human gut, and extreme environments in subsequent chapters rested more upon molecular methods than visual interrogation, yet even the latest technology is lacking. If the life in my pond and my colon are beyond comprehension, what hope do we have of understanding how the open ocean works?

Progress might be accelerated by changing the culture of biology to emphasize the micro over the macro. This could be a game changer for the science, but requires a major shift in the way we teach biology. As a veteran higher educator, I have some credentials for saying that most of us have made a big mess in convincing lots of people that biology is a spectacular subject deserving their deep and lifelong engagement. I am not sure how we have failed, or how we could be doing a better job, but here’s an example of the problem. The point of the customary microscopy class at the beginning of a biology lab course is not—and should never have been—to learn to use the microscope. It is an entrée to the student’s inquiry into the nature of life. 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. There is something rotten in the state of Denmark, and everywhere else, when a student yawns when introduced to the microscope. A common exercise in this class is to have the eager scholars swab their mouths and view their globs of mucilage on glass slides. Among the debris they can see buccal cells rubbed from the epidermis on the inside of their cheeks. These are large, flattened cells with prominent nuclei, looking like fried eggs because—which is worth reminding students—chicken eggs are single cells too. The exercise, if approached without cynicism, should counter ennui. Look at that beautiful cell: some of the fine granules are mitochondria that you inherited from your mother; the nucleus houses your 46 chromosomes; you are looking at the stuff of yourself; there is nothing more to you, nor anything less, than what you spy through these eyepieces. The fact that this experience is so often underwhelming is an educational heartbreak, or, at least, an opportunity missed.

The curriculum in the majority of degree programs in the biological sciences emphasizes human biology and the biology of our close vertebrate relatives. The same is true of high-school curricula, and the prominence given to hairy, feathery, and scaly things has always been a fact of science education. In addition to the biomolecules, metabolism and physiology, and genetics and evolution, most introductory biology courses at colleges and universities include a section on biodiversity in which the characteristics of different groups of organisms are described. The time dedicated to each slice of life varies according to the textbook used in the course and the interests of the professor. The fungi may get one lecture if they are lucky. Another class is dedicated to the bacteria, and, often, archaea and viruses are bundled into the same session. Exceptions abound, but this balance of topics parallels the coverage of biology in the best-selling introductory texts on college biology. The organismal part of the course is a gross misrepresentation of the facts of life.

I've previously  referred to plants as vehicles for their cyanobacterial chloroplasts. Pursuing this metaphorical line, there is some merit in thinking about “The Selfish Bacterium” as an analog to Richard Dawkins’ popularization 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. (I have a colleague whose curiosity about intelligent design survived Darwin, only to be crushed when he learned about the endosymbiotic origin of the eukaryote cell.) Even then, the agnostic biologist spends more of the time worrying about her daughter’s dental appointment than she does reveling in the fact that everyone in her family is energized 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 well-being, 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. The more we learn about the theater of our peristaltic cylinder, the more we lose the illusion of control. 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. In his fascinating book, "The Limits of Self," French philosopher Thomas Pradeu examined the ramifications of modern immunological theory on the concept of the individual. Much of his argument hinges on the ways in which our microbiome transforms us into chimeric organisms whose functions are integrated by the immune system.

More than 30 years ago, approaching the British equivalent of high-school graduation, I often escaped the school with a girlfriend and wandered around a community garden. Do not imagine Hogwarts for one second; and, worse, ours was a mostly miserable companionship sustained only by the certainty that this was a teenage misfortune from which the future promised deliverance. We called our refuge what we thought it did not resemble: The Garden of Eden. This triangle of grass was ringed by spindly trees that attracted chattering sparrows, and the birds drew the attentions of grimy cats; old men with gray faces shuffled around the garden too, smoking cigarettes while their dogs exercised; candy wrappers and empty bottles decorated the grass. It was an ugly little place at the bottom of a slope beneath a busy road. Calling this Eden was our satire upon the dearth of beauty in our lives.

In this twenty-first century, I have my Ohio woods in spring, washed with the colors of flowers and animated by the buzz of pollinating insects. Some of the apparent differences between the community garden and the Midwestern woods are an illusion. The beauty of a forest imposes itself on us through the look, smell, sound, and feel of its plants and animals. Its wider significance—the activities that sustain humanity—lies elsewhere, in the functioning of an intact ecosystem and its power to cleanse the air and purify the groundwater. This, like the microorganisms that perform much of the work, is invisible. The evident sensuality of the forest as well as its hidden functions are both important things from our perspective; important because the woods have the power to elevate our feelings, boost our mood, and because without them, our species cannot prosper.

Excerpted from “The Amoeba in the Room: Lives of the Microbes” by Nicholas P. Money. Copyright © 2014 by Nicholas P. Money. Reprinted by arrangement with Oxford University Press, a division of Oxford University. All rights reserved.

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