Microbial Inhabitants of Humans

The indigenous microbiota (or “normal microflora”) comprises those microbes that inhabit the healthy human body. Many of these organisms (e.g., Streptococcus pyogenes, Staphylococcus aureus, Neisseria meningitidis, Haemophilus influenzae, and Escherichia coli) are responsible for common, and sometimes life-threatening, infections of healthy individuals, whereas others cause disease only when the body’s defenses are impaired.

   This advanced textbook provides a unique overview of the microbial communities inhabiting those regions of the human body that are exposed to the external environment; these include the skin, eyes, oral cavity, and the respiratory, urinary, reproductive, and gastrointestinal tracts. To understand why particular organisms are able to colonize an anatomical region and why the resulting microbial community has a particular composition, an ecological approach is essential. Consequently, the key anatomical and physiological characteristics of each body site are described to show how these influence the nature of the environment at that site. The crucial roles of the indigenous microbiota in protecting against exogenous pathogens, regulating the development of our immune system and mucosae, and providing nutrients are also discussed. The involvement of these organisms in infections of healthy and debilitated individuals are described throughout, and methods of manipulating the composition of the indigenous microbiota for the benefit of human health are discussed. Microbial Inhabitants of Humans is a core textbook for advanced students taking courses in microbiology, medical microbiology, microbial ecology, and human biology.

Michael Wilson is Professor of Microbiology in the Faculty of Clinical Sciences and Head of the Department of Microbiology at the Eastman Dental Institute at University College London. He is the Editor-in-Chief of the journal Biofilms and has coauthored or edited several books, including Bacterial Disease Mechanisms (2002), Bacterial Adhesion to Host Tissues (2002), and Medical Implications of Biofilms (2003).

Microbial Inhabitants
of Humans

Their ecology and role in health and disease

Michael Wilson
University College London

PUBLISHED BY THE PRESS SYNDICATE OF THE UNIVERSITY OF CAMBRIDGE
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CAMBRIDGE UNIVERSITY PRESS
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© Michael Wilson 2005

This book is in copyright. Subject to statutory exception
and to the provisions of relevant collective licensing agreements,
no reproduction of any part may take place without
the written permission of Cambridge University Press.

First published 2005

Printed in the United States of America

Typefaces Swift Light 9.5/13 pt. and Gill Sans   System LATEX 2_e   [TB]

A catalogue record for this book is available from the British Library

Library of Congress Cataloguing-in-Publication Data available
Wilson, Michael, 1947-
    Microbial inhabitants of humans : their ecology and role in health and disease / Michael Wilson.
      p.  cm.
    Includes bibliographical references and index.
    ISBN 0-521-84158-5
    1. Body, Human – Microbiology.  2. Medical microbiology.  3. Microbial ecology.
   I. Title.

ISBN 0 521 84158 5 hardback

For Andrew, Bernie, Caroline, Fionn, Margaret, Mike, Pippa, Richard,
Sarah, and Wil

Long may your symbionts protect you

Contents

Preface

The Guiness Book of Records and the Hitch Hikers Guide to the Galaxy are both books that document many astounding facts concerning life, the universe, and everything else. However, as far as I am aware, in neither of these eminent publications is there any mention of two truly amazing observations: an adult human being consists of ten times as many microbial cells as mammalian cells, and he or she carries around approximately 1.25 kg of microbes. Knowing this, who could fail to be intrigued by the microbial component of that mammal–microbe symbiosis known to us as a “human being.” The immediate questions prompted by this knowledge are usually along the lines of: (1) Which microbes are present? (2) How do they manage to survive? (3) What are they doing there? (4) Are they dangerous? Each of these questions about our “indigenous microbiota” is addressed in this book, and some of the answers will be surprising.

   The complexity of the microbial communities found at many body sites is truly astounding; it has been estimated that we provide a home for at least 1,500 different microbial taxa that collectively contain more than 200 times as many genes as the human genome. Most of these organisms have not yet been grown in the laboratory, and so we know very little about them. However, modern molecular approaches are not only enabling us to detect their presence but, thanks to gene sequencing, also to gain some idea of their physiology and virulence potential. In order to try to understand how members of the indigenous microbiota manage to survive on our body and what they are up to while living there, an ecological approach has been adopted in this book – motivated by Pasteur’s statement that, “The germ is nothing. It is the terrain in which it is found that is everything.”

   As for the question of the ability of such microbes to cause disease – the answer is a resounding “yes.” Some of the deadliest diseases of humankind are caused by microbes that are normal inhabitants of various body sites of healthy individuals (e.g., Neisseria meningitidis, Streptococcus pyogenes, Haemophilus influenzae, Staphylococcus aureus, and Streptococcus pneumoniae). Amazingly, for most of our lives, the majority of individuals suffer no ill effect from harboring such organisms. Less virulent members of the indigenous microbiota are also a frequent cause of less life-threatening’ but nevertheless debilitating diseases. In fact, the most common infectious diseases of mankind – caries, periodontal diseases, and urinary tract infections – are all caused by microbes indigenous to humans. Furthermore, advances in medicine and surgery have resulted in the increasing use of various devices and immunosuppressive therapies which have provided opportunities for many indigenous microbes to cause a variety of serious infections.

   However, all is not doom and gloom, and it is important also to consider a question that is not often asked about our indigenous microbiota: Are they of any benefit? The answer, undoubtedly, is “yes.” Not only do our indigenous microbiota protect us against exogenous pathogenic microbes, but they also provide us with as much as 10 percent of our energy requirements, supply a range of vitamins, and play a key role in the development of our immune system and mucosal surfaces.

   Disappointingly, but not surprisingly, the attention that has been given to most members of the indigenous microbiota (other than disease-inducing species) by microbiologists and immunologists is insignificant compared with that directed toward exogenous pathogens. This has left us remarkably ignorant of the most intimate relationship that any of us will ever experience during our lifetime. The exhortation to “know thyself ” must surely extend to that part of the human–microbe symbiosis (i.e., our symbionts) that can justifiably be termed “microbial self.” It is the author’s hope that this book will inspire others to take a greater interest in, as well as to cherish, our indigenous microbiota.

Abbreviations used for microbial genera