Understanding the Gut Microbiota

Gerald W. Tannock

• Publisher: Wiley
• Year: 2016
• ISBN:
  9781118801345
• Edition: 1
• Topic: Biological Sciences
• Subtopic: Microbiology
• Index: Biological Sciences

This book discusses the community of microbial species (the microbiota, microbiome), which inhabits the large bowel of humans. Written from the perspective of an academic who has been familiar with the topic for 40 years, it provides a long-term perspective of knowledge about this high profile and fast-moving topic. Building on general ecological principles, the book aims to help the reader to understand how the microbiota is formed, how it works, and what the consequences are to humans.

Understanding the Gut Microbiota focuses on conceptual progress made from studies of the human bowel microbiota. Where appropriate, it draws on knowledge obtained from other animal species to provide conceptual enlightenment, but this is essentially a book about humans and their bowel microbes. Particular research approaches are recommended to fill knowledge gaps so that fundamental ecological theory and information about the microbiota can be translated into benefits for human health. The relationship between food for humans and resulting food for bowel bacteria emerges as an important topic for consideration.

This concise scholarly treatise of the microbiota of the human bowel will be of great interest and use as a text and reference work for professionals, teachers and students across a wide range of disciplines, including the health sciences, general biology, and food science and technology. The provision of handy 'explanation of terms' means that those with a general interest in science can also read the book with enjoyment.

Chapter 1
Introduction

This book is about the collection of microbes that inhabit the human colon. I became interested in the lives of gut bacteria when an undergraduate student at the University of Otago in Dunedin, New Zealand. During university vacations, I was employed as a “supernumerary” in the Department of Agriculture Veterinary Diagnostic Laboratory, Invermay Agricultural Centre, which is close to Dunedin. Not always rushed off my feet with laboratory work, I enjoyed the opportunity to occasionally browse the library literature, especially new journal articles. One day, I stumbled upon an article by René Dubos and his colleagues at Rockefeller University, New York on the subject of bacteria in the gut of mice. I found that there was a whole series of papers^1–5 from this group in the Journal of Experimental Medicine, and that some of them described experiments that used germfree animals. The articles really excited me, and led me to suggest a fourth-year Honors project on lactobacilli and porcine stomachs to Sandy Smith (who later became my PhD supervisor). I soon realized that the Rockefeller research was the first application of “microbial ecology thinking” to gut bacteriology.

One of the authors of the Rockefeller papers was Dwayne C. Savage. A particular paper,⁵ of which he was first author, described the association of bacteria with epithelial and mucosal surfaces in the gut of mice. It so bowled me over that eventually I became a Fogarty International Postdoctoral Fellow in Dwayne's laboratory, first in Texas and then in Illinois. Dwayne's excellent mentoring set me on the career-long path of microbiota research that I have enjoyed ever since.

One of the thrilling sites that I saw in histological sections in the laboratory during my years in the United States was a layer of lactobacilli colonizing the epithelial surface of part of the murine stomach. It led me to spend much time in subsequent years investigating, with the help of a unique colony of Lactobacillus-free mice and some splendid laboratory associates, how a particular strain of Lactobacillus reuteri manages to live in the anterior gut of mice.

In 2001, Dwayne wrote a fine article for Current Issues in Intestinal Microbiology entitled “Microbial Biota of the Human Intestine: A Tribute to Some Pioneering Scientists.”⁶ It is worth reproducing the Abstract here, because it reminds us that much excellent research concerning gut bacteria was accomplished as long ago as the 1960s. It gives us some perspective on the topic:

Research on the indigenous intestinal microbiota of man was initiated well before the end of the 19th Century. The work continued at a slow but steady pace throughout the first half of the 20th Century. Findings from the effort had little impact on medicine and other aspects of human biology, however, until the 6th decade of the 20th Century. During that decade, research in the area was begun by eight groups of investigators, each of which was led by one or two senior scientists with great experimental talent, creativity and foresight. Their findings added new dimension to knowledge of the microbiota and initiated an explosion of interest in research in the field that has continued to the present day. The research of the groups during the 1960's is described in this review as a tribute to the senior scientists who had such critical impact on this important field of study.

Dwayne first pays tribute to Theodore Escherich,⁷ who, more than 100 years ago, recognized, “At a time when microbiologic research has gained us so many laurels by following the research methods of Koch into the regions of the etiology and pathology of infectious diseases, it would appear to be a pointless and doubtful exercise to examine and disentangle the apparently randomly appearing bacteria in normal feces and the intestinal tract, a situation that seems controlled by a thousand coincidences. If I have nevertheless devoted myself now for a year virtually exclusively to this special study, it was with the conviction that the accurate knowledge of these conditions is essential, for the understanding of not only the physiology of digestion, but also the pathology and therapy of microbial intestinal diseases.” He then records the contribution of Theodore Rosebury,⁸ who provided a summary of the research undertaken from the 19th century through to the 1960s in his book, Microorganisms Indigenous to Man. The remainder of the review describes the eight groups of scientists whose work in the 1960s transformed microbiological and medical attitudes to the “normal flora” of the human gut. I, too, will list these heroes of gut microbiota research and summarize their contribution to the field – it is important to remember that we are “dwarfs standing on the shoulders of giants,” and that our ability to understand a topic more deeply than our predecessors is not because we are smarter, but because we are lifted up by, and building on, their achievements:

• B. S. Drasar and colleagues (UK).⁹ The association of bowel bacteria with certain diseases, the role of pH and peristalsis as regulatory factors in bowel ecology.
• René Dubos, Russell Schaedler, Dwayne Savage, and colleagues (USA).^{10, 11} Development of probably the first specific-pathogen-free (SPF) mouse colony, culture of previously unknown gut bacteria, impact of gut commensals on host physiology, association of bacteria with gut surfaces, a “microbial ecological” view of the gut ecosystem (symbiosis, biological succession).
• Sherwood Gorbach and colleagues (USA).¹² Sampling gastric and small-bowel contents, culture of commensals from these sites, investigation of diarrheal diseases, proponent of probiotics.
• Bengt Gustaffson, Tore Midvedt, and colleagues (Sweden).¹³ Gnotobiotic animal experiments, description of physiological and anatomical differences between germfree and conventional animals, the microbiota as “the most cell-rich biochemically active organ” of the human body.
• Helmut Haenel and colleagues (German Democratic Republic).¹⁴ Culture-dependent studies of the fecal microbiota in childhood.
• Tomotari Mitsuoka and colleagues (Japan).¹⁵ Innovative culture methods for anaerobic bacteria, comparisons of microbiota composition in humans and other animals, changes in microbiota composition with respect to aging.
• Pierre Raibaud, Robert Ducluzeau, and colleagues (France).¹⁶ Innovative culture-dependent studies of commensal bacteria, gnotobiotic animal experimentation involving defined mixtures of cultivated bacterial species, the fecal microbiota in early life.
• H. Williams Smith (UK).¹⁷ Comparative acquisition of the gut microbiota of farm animals using culture-dependent methods, relative abundances of bacterial groups present in various levels of the gastrointestinal tract.

The combined contributions of these clinicians and scientists led to the following conclusions about the gut microbiota:

• The microbiota of healthy adult humans is composed of bacteria that are able to live anaerobically.
• Hundreds of bacterial species make up the fecal microbiota; a small proportion of the inhabitants of the bowel are Archaea that produce methane.
• The distal small and large bowels contain diverse and abundant bacterial species.
• Transient bacteria ingested with food and inhabitants of the upper digestive tract can be detected in feces along with the colonic microbiota members.
• The colonic microbiota contains trillions of bacterial cells.
• The microbiota contributes to about 50% of fecal mass.
• A biological (ecological) succession occurs in the bowel during early life.
• Some commensals are associated with the mucus covering the bowel epithelium, at least in some animal species and conditions.
• The microbiota is regulated by host-associated factors ...