Trends in the Systematics of Bacteria and Fungi

Paul Bridge, David Smith, Erko Stackebrandt, Paul Dennis Bridge, David Smith, Erko Stackebrandt

• Publisher: CAB International
• Year: 2020
• Print ISBN:
  9781789244984
• eBook ISBN:
  9781789245004
• Topic: Scienze biologiche
• Subtopic: Biologia

Methods in microbial systematics have developed and changed significantly in the last 40 years. This has resulted in considerable change in both the defining microbial species and the methods required to make reliable identifications. Developments in information technology have enabled ready access to vast amounts of new and historic data online. Establishing both the relevance, and the most appropriate use, of this data is now a major consideration when undertaking identifications and systematic research.This book provides some insights into how current methods and resources are being used in microbial systematics, together with some thoughts and suggestions as to how both methodologies and concepts may develop in the future. It includes coverage of: The philosophy and changes in microbial systematics, including the relevance of names, new concepts of species, and the issues encountered with species that cannot be grown in culture.The application of new identification technologies, specifically those based on nucleic acids and complex chemo-taxonomic methods.The challenges of using published databases and other data resources in arriving at an identification appropriate to current species concepts.The practical requirements of an identification: obtaining and verifying reference cultures and data, and the type and level of identification required by different users.This book is suitable for academic researchers, scientists involved with identification or survey, microbiologists, students and extension workers.

1 Bridging 200 Years of Bacterial Classification

Ramon Rosselló-Móra¹ and Erko Stackebrandt^2*

¹Grup de Microbiologia Marina, Department Animal and Microbial Diversity, IMEDEA (CSIC-UIB), Esporles, Spain; ²Kneitlingen, OT Ampleben, Germany

^*[email protected]

Introduction

The history of bacterial systematics reflects scientific progress in which approaches (often developed in non-biological disciplines) were adopted to improve the accuracy of bacterial taxonomy and to develop comprehensible relationships. What started two centuries ago with a blurred vision of the simplest properties of the bacterial cell became more focused once pure cultures were achievable. At an amazing speed, their existence as both harmful pathogens for humans, plants and animals and as beneficial partners in agriculture, food and industrial applications was disclosed. Microbiology as a scientific discipline in its own right was established, although the historical connection to botany was still recognizable until recently. In parallel with the enormous avalanche of strains, names and accompanying data already generated at the dawn of microbiology, attempts were made to understand the origin of bacteria, and to order them into a system that depicted the relationships among themselves and to other living organisms. A large number of systems were outlined with hardly any of them being identical to another. It was not until far into the 20th century that two major events occurred that would change our perception of how to reject the plethora of bacterial names and classification systems. The first was the establishment of the Approved List of Bacterial Names (Skerman et al., 1980) that brought order into the huge number of synonyms based on obscure species descriptions; the second was the perception that proper classification needed to be based upon phylogenetic relationships. Within a short period of 20 years the tree of life began to unfold, and what originally was founded on a single evolutionary conservative gene has now been extended to genome sequences. Moreover, the era in which pure cultures were needed to assess phylogenetic novelty has been extended to the direct application of metagenome and microbiome studies to environmental samples. As a result, the ‘traditional’ bacteriologists are confronted with the interest of ‘molecular systematists’ in giving names to as yet uncultured organisms and even to genomes or fragments thereof. No doubt, without a mutual understanding of the rationale and purpose of naming the individual entities (from genes to cultured cells) confusion is bound to occur, especially if different entities of a given organism are named differently. This chapter will briefly take a historical view of the major steps in bacterial systematics leading to the first reconciliation workshop in 1987 and a re-evaluation of the species concept in 2002. New challenges and concepts developed since then will be outlined.

The Historical Perspective

The changing consideration of bacterial taxonomic assessment

The early era

Microorganisms became visible by means of the introduction of Antony van Leeuwenhoek’s microscope in the mid-17th century. He and Lazzaro Spallanzani objected to the idea of spontaneous generation of microorganisms, and paved the way for the future development of the science of microbiology. It took about another 100 years before the first report on classification and characterization of microorganisms was attempted (Müller, 1786). Another century of optical and instrumental improvement passed before the name ‘Bacterium’ as a genus was introduced as a scientific word by Christian Gottfried Ehrenberg (1838). As Ehrenberg stated: ‘eine Milchstrasse der kleinsten Organisation geht duch die Gattungen Monas, Vibrio, Bacterium…’ (‘a Milky Way of the smallest organization runs through the genera Monas, Vibrio, Bacterium…’). However, while at that time their occurrence and relationships in different niches became apparent to the early microbiologists, neither their ecological function nor their mutual relationships revealed themselves to the observer.

It is a part of human nature to arrange subjects into categories, no matter how small the number and how difficult the selection criteria. Being mostly botanist by education is not surprising that, in the absence of facts about their phylogeny, the nature of bacteria (based on nothing more than basic morphological descriptions) could not be properly evaluated by these early systematists. The apparent similarity of mainly unicellular forms and separation by fission allowed the early microbial systematists to deduce that bacteria derived from animals (van Leeuwenhoek, Müller, Ehrenberg), and later from fungi, classifying them as Schizophytae (Cohn, 1872), a system in which bacteria were placed together with ‘Spaltalgen’ (today named cyanobacteria).

This early period which Paul de Kruif (1926) characterizes so well in his famous novel Microbe Hunters is dominated by discoveries in the medical field. But this era also saw the exploration into other scientific fields, such as immunology, chemotherapy, physiology, industrial microbiology, biochemistry and the study of metabolisms, leading to a rapid growth in knowledge about the properties of microorganisms and their interactions with biotic and abiotic matter.

In the second half of the 19th century the deposition and exchange of microbial cultures; the organization of international conferences; and the accessibility of scientific literature was limited, and it is not surprising that individual systematists generated a plethora of systems. Migula (1900) compared about 30 such systems, published between 1836 and 1894. At the dawn of microbiology, and even later, the same microorganism was given different names as individual researchers based their taxonomy on different properties. It was not until 1980 that the Approved List of Bacterial Names (Skerman et al., 1980) brought nomenclatural order into bacteriology by starting a new date for bacterial nomenclature. The tens of thousands of names for bacterial species were reduced to about 2500 names that could be linked unambiguously to a previously defined name of a bacterial species. Nevertheless, despite the methodological shortcomings of taxon descriptions, the early 19th century must be considered a period of great scientific achievement and accurate observations, as some of the names given to bacteria with particular morphologies in the first half of the 19th century (e.g. Spirillum [Ehrenberg, 1835], Spirochaeta [Ehrenberg, 1835] and Sarcina [Goodsir, 1842]) were recognized as valid and included in the Approved List.

To recognize the historic development of species characterization and the changes in affiliating genera to higher taxa we use the fate of Vibrio cholerae as an example, starting from the first description by Filipo Pacini (1854) through a series of progress reports as laid down in Bergey’s Manual of Determinative Bacteriology and later of Bergey’s Manual of Systematic Bacteriology. Almost any other taxon described before the late 20th century was prone to the same fate as the genus Vibrio and its type species V. cholerae.

A witness of scientific progress: Bergey’s Manual of Determinative Bacteriology

About 20 years after the publication of Ehrenberg (1832) a Vibrio-shaped bacterium was deduced as the most likely causative agent of cholera disease and was named V. cholerae by Pacini (1854), although for several decades Robert Koch was listed as the discoverer of this bacterium. For some of the reasons indicated above, strains of this species or similar organisms were named (among others) Bacillus cholerae-asiaticae (Pacini, 1854) Trevisan, 1884; Spirillum cholerae-asiaticae (Trevisan, 1884) Zopf, 1885; Microspira comma Schröter, 1886; Spirillum cholerae (Pacini, 1854) Macé, 1889; Vibrio comma (Schröter, 1886) Blanchard, 1906; or Liquidivibrio cholerae (Pacini, 1854) Orla-Jensen, 1909 (see www.bacterio.net/vibrio.html, accessed 4 July 2020).

After World War I the dominance of microbial systematics and taxonomy shifted from Europe to the USA. Initiated by the Society of American Bacteriologists, David Hendricks Bergey was appointed chairman of an editorial board in charge of publication of a Manual; under the name Bergey’s Manual of Determinative Bacteriology, this book and its several editions remained the international reference work and benchmark for bacterial taxonomy. Since 1923 this Manual has served as the main data depository for identification and systematics. No other textbook on bacterial properties is a more accurate witness of taxonomic innovation and progress in identification. Its editors chose a useful, reasonably stable, artificial classification rather than trying to place systematics within a phylogenetic framework (cited in Sapp, 2005). This was not, however, consequently put into practice, as seen in the affiliation of the genus Vibrio with the family Spirillaceae in the 1st edition (Bergey et al., 1923). The number of properties included for V. comma (first Koch, then Schröter were given as references) is small and restricted to culture observations such as shape, flagellation, reaction of growth and pigmentation in different media, a few physiological properties and habitat. The name and taxonomic affiliation, as well as the descriptive criteria, remained basically unchanged in the 2nd to the 5th edition (Bergey, 1925, 1930, 1935; Bergey et al., 1939), except that the genus Vibrio was placed in the family Pseudomonadaceae in the 5th edition and in the listing of a few more physiological reactions (acid production from carbohydrates). The stagnation seen in microbial taxonomy in the first 30 years of the 20th century contrasts with the progess witnessed in the ‘Golden Age of Microbiology’ before and around the turn of the 19th century. Although DNA was discovered around 1860, bacterial transformation experiments were published in the 1920s, and chromosomes were identified as the cellular structures responsible for heredity, the structure of DNA had still not been deciphered and genetics was in its infancy. The absence of a clearly defined nucleus let Copeland (1938) propose a separate kingdom – Monera – for the bacteria (and cyanobacteria), bringing them to the same level as those of animals, plants and protoctista. A historic view on the development of the highest systematic ranks (kingdoms, domains) and a summary of the thoughts of leading scientists on the likeliness (and purpose) of constructing a phylogenetic framework for bacteria has been given by Sapp (2005). The 1940s and 1950s saw the development of electron microscopy; the evidence that DNA, not protein, is the genetic material; and the double helix structure of DNA was proposed. As progress in these scientific eras was not evaluated for application in bacterial systematics, the range of taxonomic properties remained basically the same until the early 1970s. van Niel’s statement (1955) about the inappropriateness of phenotypic data to order taxa into a hierarchic system and to replace the binominal system of species by common names is a clear testimony to the frustration with bacterial classification prevailing in these decades.

Still concentrating on the cultural properties of V. comma, the description of this species in the 6th and 7th editions (Breed et al., 1948 and 1957, respectively) were almost identical but included physiological properties additional to those in the previous editions. More important, information on the antigen structure (O, somatic and H, flagellar) led to the clustering of V. cholerae strains into groups and subgroups. While in the 6th edition the genus Vibrio was affiliated to the family Spirilleae, it was a member of the family Spirillaceae in the 7th edition.

The 1960s and 1970s saw a boom in the introduction of taxonomic methods, ranging from the molecular (DNA-DNA and DNA-rRNA hybridization, mol% G+C of DNA) over chemotaxonomic (peptidoglycan, fatty acid, isoprenoid quinone, lipid A, polar lipid) to the phenotypic level (numerical taxonomy) as well as the design of novel cultivation strategies (anaerobic techniques). Naming the key authors of these many approaches would be beyond the framework of this chapter (see Chapters 9, 10, 13, 15 and 16). However, Sokal and Sneath (1963) should be mentioned here, as computer-assisted numerical taxonomy was the favoured classification of microbes of the 1960s and 1970s. The need to optimally characterize bacterial isolates by the ...

Table of contents

• Cover
• Half Title
• Title
• Copyright
• Contents
• List of Figures
• List of Tables
• List of Authors
• Preface
• Chapter 1 Bridging 200 Years of Bacterial Classification
• Chapter 2 Identification of Fungi: Background, Challenges and Prospects
• Chapter 3 Names of Microorganisms and Data Resources to Retrieve Information about Published Names
• Chapter 4 Preserving the Reference Strains
• Chapter 5 Can Older Fungal Sequence Data be Useful?
• Chapter 6 Data Resources: Role and Services of Culture Collections
• Chapter 7 MALDI-TOF MS and Currently Related Proteomic Technologies in Reconciling Bacterial Systematics
• Chapter 8 MALDI-TOF MS and its Requirements for Fungal Identification
• Chapter 9 The Strength of Chemotaxonomy
• Chapter 10 Microbial Genomic Taxonomy
• Chapter 11 Navigating Bacterial Taxonomy in a World of Unchartered Microbial Organisms
• Chapter 12 Sequence-based Identification and Classification of Fungi
• Chapter 13 Identification and Classification of Prokaryotes Using Whole-genome Sequences
• Chapter 14 Genomic Sequences for Fungi
• Chapter 15 What can Genome Analysis Offer for Bacteria?
• Chapter 16 Genomes Reveal the Cohesiveness of Bacterial Species Taxa and Provide a Path Towards Describing All of Bacterial Diversity
• Chapter 17 Are Species Concepts Outdated for Fungi? Intraspecific Variation in Plant-pathogenic Fungi Illustrates the need for Subspecific Categorization
• Chapter 18 Where to Now?
• Appendix
• Index
• Cabi
• Back