At the close of the 1970s, the two-domain classification scheme long used by most biologists—prokaryotes versus eukaryotes—was upended by the discovery of an entirely new group of organisms: archaea. Initially thought to be bacteria, these single-celled microbes—many of which were first found in seemingly unlivable habitats like the volcanic hot springs of Yellowstone National Park—were in fact so different at molecular and genetic levels as to constitute a separate, third domain beside bacteria and eukaryotes. Their discovery sparked a conceptual revolution in our understanding of the evolution of life, and Patrick Forterre was—and still is—at the vanguard of this revolution. In Microbes from Hell, one of the world’s leading experts on archaea and hyperthermophiles, or organisms that have evolved to flourish in extreme temperatures, offers a colorful, engaging account of this taxonomic upheaval. Blending tales of his own search for thermophiles with discussions of both the physiological challenges thermophiles face and the unique adaptations they have evolved to live in high-temperature environments, Forterre illuminates our developing understanding of the relationship between archaea and the rest of Earth’s organisms. From biotech applications to the latest discoveries in thermophile research, from microbiomes to the communities of organisms that dwell on deep-sea vents, Forterre’s exploration of life-forms that seem to thrive at the mouth of hell provides a glimpse into the early days of Earth, offering deep insight into what life may have looked like in the extreme environments of our planet’s dawn.
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About the Author
Patrick Forterre, former head of the Microbiology Department at the Institut Pasteur, is presently professor at the Institut Pasteur and professor emeritus at the Université Paris-Saclay, France. Teresa Lavender Fagan is a freelance translator living in Chicago; she has translated numerous books for the University of Chicago Press and other publishers.
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Microbes from Hell
By Patrick Forterre, Teresa Lavender Fagan
The University of Chicago PressCopyright © 2016 The University of Chicago
All rights reserved.
A Bit of History: Microbes and Humans
Microbes from hell ... Everyone has heard of microbes, and almost everyone has a vague idea of what the term represents: very small creatures that can do a lot of harm. If they're in hell, why not let them stay there? To get to the heart of the subject, we'll have to move beyond these prejudices, get to know microscopic life better, and look a little more closely at what the word "microbe" really means.
Did You Say "Microbe"?
For a long time, our knowledge of the living world was limited to macroscopic organisms — that is, those visible to the naked eye. The living world was generally divided into two groups: animals and plants. It was only in the seventeenth century, with the invention of the microscope, that the Dutch clothing manufacturer and microscope maker Antonie van Leeuwenhoek (1632–1723) discovered the existence of the then unimaginable world of microscopic living creatures. Two centuries later, Charles Sedillot, a contemporary and colleague of Louis Pasteur, would dub them "microbes," from the Greek bios for "life" and mikros for "small" (figure 1.1a).
Their sizes proved to vary considerably, with the largest among them measuring a few tenths of a millimeter in length and the smallest being no bigger than a micron (less than a thousandth of a millimeter). Very soon it appeared that these minuscule beings, invisible to the naked eye (or even the most powerful magnifying glass), were present everywhere: in water, in the air, in the ground, and even in the human body. In the nineteenth century, people were frightened to realize that these microbes, far from representing just a simple curiosity of nature that could be ignored, were the cause of many of the scourges that had stricken humanity for centuries: plague, typhus, tuberculosis, syphilis, and so on. Today we know that most microbes are innocent, and some are even our benefactors — in particular, those that live in our intestines and protect us from attacks by their pathogenic siblings (other microbes that are responsible for illnesses) and those that help us digest food. In the past few years, after sequencing the human genome, scientists have focused on the sequencing of the genomes of all microbes — the "microbiome." In fact, we contain ten times more microbial cells than human cells; these microbes belong to a considerable number — several thousand — of different species. Scientists have recently discovered that these microbes might even manipulate the brain: for example, by producing molecules that make us want to eat what they need. If we get to know them better and learn to manipulate them in turn, we should be able to derive enormous benefits in the realm of human health. Nevertheless, the term "microbe" in the collective subconscious retains a rather fearsome connotation. (I hope that after reading this book you will have changed your mind a bit.)
In general, biologists no longer use the word "microbe" (perhaps due to its rather pejorative nature, or because it doesn't sound very scientific). Instead, they use the word "microorganisms" to describe the living beings that can be observed only under a microscope. For a long time, scientists were unable to situate these organisms in relation to other representatives of the living world. They even tried to force them into the old traditional framework by seeking characteristics in their appearances that might connect them to animals or plants. If a microbe was able to move on its own, thanks to a flagellum, it was a minianimal, and it became a subject of study for zoologists. If, on the contrary, it remained immobile most of the time and was made up of a cell surrounded by a thick wall, it was a miniplant, and was of concern to botanists. It was from that time that biologists, in order to name microbes, began to use binomial nomenclature (in which every living being is designated by a genus name and a species name), invented in the seventeenth century by the great Swedish naturalist Carl von Linné (Linnaeus) for animals and plants. For example, the bacterium responsible for plague was named Yersinia pestis, a name that recalls the illness for which it is responsible and honors the one who discovered it: Pasteur's young colleague Alexander Yersin. The name of the bacterium used as a model by many biologists, Escherichia coli (commonly called E. coli), recalls its preferred habitat, our colon, and honors another microbiologist, Theodor Escherich, who was working in Vienna at the beginning of the twentieth century.
A decisive tool in the study of microbes, the petri dish (figure 1.1d), was invented in the 1880s in Germany by the team of Pasteur's German rival, Robert Koch, who discovered Mycobacterium tuberculosis, responsible for tuberculosis. The story goes that it was while observing colonies of bacteria and mushrooms on the surface of slices of potatoes, the leftovers of a meal eaten quickly between two experiments, that the German scientists understood that each colony (circular spots of varying size, of different colors, whose edges were more or less sharp) corresponded to a clone of billions of microbes, all of which came from a single cell, bacterium or mushroom, that had settled on the surface of the potato. Julius Richard Petri, one of Koch's assistants, had the idea of filling a circular glass dish with a jellylike substance, agar, containing a culture medium to obtain bacterial colonies isolated on the surface of the agar (figure 1.1d). He had only to dilute the bacterial cultures sufficiently to place a few bacteria on the petri dish. This method, still used today, makes it very easy to isolate pure cultures of bacteria, which can then be characterized; this enables species to be defined. The glass of Petri's dishes has simply been replaced with plastic; agar, initially used by the wife of another of Koch's assistants to cover the surface of her jam jars to keep them sterile, is also used today.
Microbes Are Cells
During the nineteenth century, scientists gradually came to understand that all living beings, which at the time they classified in the category of either animals or plants, were formed by the assembly of a very great number of cells (a hundred thousand billion for a human being), with each cell forming the morphological unit — the elementary brick, in a sense — of the living parts of organisms. Observed under an optical microscope, the cells appeared as masses of a gelatinous substance (cytoplasm) surrounded by a thin membrane and containing a spherical central region enclosing nucleic acids (observed by using certain dyes): a sort of nucleus. Animals, plants, most algae, and mushrooms were thus formed by a great variety of organs and tissue, with each tissue composed of myriad cells. It was then noted that most microbes were formed by a single cell. Alongside the division of the living world into animals and plants, a division between multicellular (what I sometimes call macrobes) and single-celled organisms (microbes) came to be superimposed.
It quickly became obvious that single-celled organisms had an incredible variety of shapes: there was a microbe, and then there was a microbe. The largest could resemble animal or plant cells that had been able to live in an isolated state. This was, for example, the case of the paramecium, which, with its single cell endowed with two orifices — one serving as a "mouth," the other as an "anus" — seemed to sum up the functions of a complete animal organism. Such living beings, which are grouped under the term "protists," were for a long time considered to be small, primitive animals or plants — protozoa and protophyta, respectively. Other microbes, such as yeasts, presented characteristics common to mushrooms, while still others were similar to algae. Alongside these miniature animals or plants were even smaller microbes, already observed by Van Leeuwenhoek, that could not be connected to any group of organisms visible to the naked eye. These "minimicrobes," although visible under the optical microscope, were so small that using traditional optical microscopes to distinguish any details inside the single cell that formed them was impossible (figure 1.1b). In particular, it was difficult to distinguish a nucleus in these miniature microbes. The most characteristic among them had the shape of a stick — hence their name, "bacterium," from the Greek term bakteria, which means "stick." Subsequently, all extremely small microorganisms formed by a cell of this type were called bacteria, regardless of their shape: stick, tendril, sphere, or filament. Until the end of the nineteenth century, botanists associated bacteria with plants, owing to their thick cellular wall. During my studies at the Faculté des Sciences in Paris, in 1969, I heard of bacteria for the first time in a course in plant biology — proof that in matters of classification of living beings, ideas can take time to evolve. We will soon see that bacterial cells are quite different from plant cells.
Enter the Viruses
Toward the end of the nineteenth century, a new class of microbes made a surprise appearance: viruses (a Latin word that means "poison"). These microbes, responsible for infectious illnesses, were so small that they could not be observed under optical microscopes. Then how were they detected? It was noticed that, even after filtration through the holes of porcelain filters capable of retaining the smallest bacteria known at the time, the secretions of plants or animals afflicted with certain illnesses (tobacco mosaic or rabies, for example) still contained a microbe capable of infecting another organism. In addition to their small size, viruses presented another specificity: they could not be cultured alone, unlike most of the bacteria studied in laboratories. They could reproduce only in the presence of the organism they infected. Viruses were thus obligatory parasites, but scientists didn't understand why.
At the beginning of the twentieth century, a French Canadian scientist, Felix d'Herelle, discovered viruses that attacked bacteria. He gave them the name "bacteriophages," meaning "eaters of bacteria," because at the time most of his colleagues didn't believe they were viruses. D'Herelle immediately had the idea of using these viruses to treat illnesses caused by pathogenic bacteria. A few days after discovering bacteriophages (often simply called phages) in the stool of a patient hospitalized at the Institut Pasteur who was beginning to feel better, d'Herelle was able to cure a little girl of typhoid. This was the beginning of phage therapy, a method of treating bacterial illnesses by using phages. This therapy was commonly used in the Soviet Union, but rarely in the West, in particular after the discovery of antibiotics. Today, phage therapy is coming back into fashion, owing to the growing number of dangerous pathogenic bacteria that have become resistant to multiple antibiotics. Petri's cultures, mentioned above, also played an important role in the study of phages. If you grow a film of bacteria on the surface of a petri dish (this is called a lawn) and you place a few phages on the surface of this film, you will see light spots appear. These correspond to the places where, in multiplying, the phage has gradually destroyed all the bacteria (figure 1.2e).
This is called a lysis plaque, because the bacteria have been "lysed" by the virus, meaning their cell structure has burst. This technique has, once again, enabled the definition of viral species through the pure viral cultures that have been obtained. All the same, faced with uncertainty regarding the nature of these microscopic parasites, the Linnaean binomial nomenclature was not used for viruses; instead, they received various names, most of the time associated with the illness for which they were responsible (such as the AIDS virus). Bacteriophages, which are all responsible for the same "illness" (the death of bacteria), are sometimes given names associated with the infected bacteria, or, when a bacterium was infected by different phages, are named through associations of numbers or letters (or both) that recall the conditions in which they had been isolated. We will see a few examples of this below.
When Two Primary Kingdoms Share the World of the Living
For a long time, many biologists had a tendency to consider bacteria and viruses as groups completely separate from the rest of the living world. They were both right and wrong. We had to wait until the middle of the twentieth century to realize that these microbes were composed of the same molecules as animals, plants, or mushrooms. In the 1960s, the pioneers of molecular biology were able to show that the principal processes ruling the functioning and division of a cell are the same in all cellular living beings: bacteria, protists, animals, or plants. It was at that time that the French scientist Jacques Monod, who won the Nobel Prize in Medicine in 1965 for his discovery of the regulatory mechanisms for the expression of genes, coined a famous phrase: "What is true for Escherichia coli [the model bacterium for molecular biologists] is true for the elephant." Let's briefly recall that in all living beings, the hereditary genetic data are contained, in the form of genes, in a DNA molecule (or RNA, in certain viruses). Each gene encodes the message enabling the synthesis of a protein on the level of a specialized cellular structure: the ribosome. Each protein serves a given function in the life of the cell. The genetic code, which enables the translation of the message carried by the DNA in proteins, is identical for all living beings. We will return in more detail to all these mechanisms in chapter 3.
All the same, this unity of the living world must not hide the fact that there are profound differences within it. When biologists were able to use electron microscopes (figure 1.2a) to observe microbes, they realized that the bacterial cell was much simpler than the cells of all other living beings. The cells of animals, plants, mushrooms, or large microbes (protists) are particularly complex. They contain all the specialized "cell organelles" (such as mitochondria, which are used in breathing). Observation under the electron microscope also revealed an elaborate system of intracellular membranes inside these cells. In particular, their chromosomes, which contain the genetic information in the DNA molecule, are separated from the cytoplasm by a membrane, the nuclear membrane, that delimits a specific compartment, the nucleus, which had already been observed under an optical microscope (see the two pictures of an amoeba in figure 1.3).
This compartmentalization has a very important effect: proteins are synthesized on the ribosomes located in the cytoplasm. The genetic message, contained in the nucleus, must then be transferred from the nucleus to the cytoplasm to be able to be read by the ribosomes. Molecular biologists have shown that each gene sends ribosomes a "messenger" RNA that is synthesized in the nucleus and then transported to the cytoplasm by passing through the pores located in the nuclear membrane (figure 1.3).
Bacterial cells are much simpler (and often much smaller: see figure 1.3 for an example). In general, they don't contain any organelle or intracellular membrane (as always in biology, there are exceptions), and they don't possess a "true" nucleus: their genetic material is localized in the cytoplasm, directly in contact with the machinery that creates the proteins. This proximity enables the RNA message to be read by the ribosomes in the process of its synthesis through bacterial DNA, called a coupling between the transcription (transcription of the DNA message into a messenger RNA) and translation (translation of the message into proteins; figure 1.3). We will return to these mechanisms in more detail in chapter 3.
The complex cells of animals, plants, and protists have been called eukaryotic(which literally means "true nucleus") to distinguish them from bacterial cells, including DNA, which is simply condensed at the center of the cell, forming a "pseudo" nucleus, explaining why it was difficult to observe under an optical microscope. These cells without a true nucleus have been called prokaryotic, which can mean "approximate nucleus," or, more literally, "before the nucleus."
The discovery of these two cell types within the biosphere led biologists in the 1960s to divide the living world into two large "superkingdoms": eukaryotes, including animals, plants, mushrooms, algae, and protists; and prokaryotes, containing only bacteria. This classification was quickly adopted by all biologists; very soon it was also considered to be a reflection of the history of the living world. Prokaryotes, being simpler, must have appeared first, followed much later by eukaryotes. The term "prokaryote," meaning "before the nucleus," reflects that idea. Following this hypothesis, it was noticed at the same time that the two principal types of organelles present in eukaryotic cells — mitochondria (present in almost all eukaryotes, with the exception of a few protists) and chloroplasts (present in plants and algae and responsible for photosynthesis) — came from ancient bacteria that, a very long time ago, had merged through symbiosis with the ancestors of present-day eukaryotic cells. The modern eukaryotes (with mitochondria) thus necessarily appeared after bacteria.
Very quickly, the terms "prokaryote" and "bacteria" became synonyms for most biologists. The term "prokaryote," which originally designated a type of cell structure (absence of a true nucleus), ended up taking on an evolutive connotation: all prokaryotes must be close relatives, and all descend from the same ancestral prokaryote. For many biologists, the molecular mechanisms of prokaryotes should thus greatly resemble each other, and it was sufficient to study one bacterium on the molecular level to know them all. In particular, the discoveries made from the model bacterium for molecular biologists, Escherichia coli, were to be systematically extrapolated to all bacteria. In fact, this way of thinking, still tacitly accepted today by many biologists and taught in most universities, would be proven to be completely false, as revealed at the end of the 1970s in some truly revolutionary work. We will soon discover that microbes from hell played a primary role in this affair.
Excerpted from Microbes from Hell by Patrick Forterre, Teresa Lavender Fagan. Copyright © 2016 The University of Chicago. Excerpted by permission of The University of Chicago Press.
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Table of Contents
Prologue 1 A Bit of History: Microbes and Humans 2 Hunting Hyperthermophiles and Their Viruses: From the Great Depths to the Laboratory 3 How Do You Live in Hell? 4 The Universal Tree of Life: Where to Place Microbes from Hell and Their Viruses? 5 The Universal Tree of Life: Are Microbes from Hell Our Ancestors? Epilogue Acknowledgments Notes References Index