Historical and Epistemological Perspectives on What Horizontal Gene Transfer Mechanisms Contribute to Our Understanding of Evolution

Abstract

Since the 1990s, results coming in from molecular phylogenetics necessitate us to recognize that Horizontal Gene Transfer (HGT) occurs massively across all three domains of life. Nonetheless, many of the mechanisms whereby genes can become transferred laterally have been known from the early twentieth century onward. The temporal discrepancy between the first historical observations of the processes, and the rather recent general acceptance of the documented data, poses an interesting epistemological conundrum: Why have incoming results on HGT been widely neglected by the general evolutionary community and what causes for a more favorable reception today? Five reasons are given: (1) HGT was first observed in the biomedical sciences and these sciences did not endorse an evolutionary epistemic stance because of the ontogeny/phylogeny divide adhered to by the founders of the Modern Synthesis. (2) Those who did entertain an evolutionary outlook associated research on HGT with a symbiotic epistemic framework. (3) That HGT occurs across all three domains of life was demonstrated by modern techniques developed in molecular biology, a field that itself awaits full integration into the general evolutionary synthesis. (4) Molecular phylogenetic studies of prokaryote evolution were originally associated with exobiology and abiogenesis, and both fields developed outside the framework provided by the Modern Synthesis. (5) Because HGT brings forth a pattern of reticulation, it contrasts the standard idea that evolution occurs solely by natural selection that brings forth a vertical, bifurcating pattern in the “tree” of life. Divided into two parts, this chapter first reviews current neo-Darwinian “tree of life” versus reticulate “web of life” polemics as they have been debated in high-profile academic journals, and secondly, the historical context of discovery of the various means whereby genes are transferred laterally is sketched. Along the way, the reader is introduced to how HGT contradicts some of the basic tenets of the neo-Darwinian paradigm.

Timeline

1717:

Mary Wortley Montagu introduces “variolation,” an immunizing technique against smallpox (Variola)

1798:

Edward Jenner injects cowpox as an immunizing technique against smallpox (Variola). His work avalanches a series of inoculation experiments that underlie vaccination therapy

1809:

Jean Baptiste Chevalier de Lamarck publishes his Philosophie Zoologique

1817–1828:

The fields of embryology, epigenetics, and evo-devo take off with the works of Heinz Christian Pander, Karl Ernst Ritter von Baer, and Edler von Huthorn

1837/1838:

Darwin draws the “I think” diagram in his Notebook B

1838:

Matthias Schleiden contends that all plants are made up of cells

1839:

Theodor Schwan declares that all animals are made up of cells

1848:

Wilhelm Hofmeister describes mitosis

1855:

Rudolf Virchow declares that all cells come from pre-existing cells

1859:

Darwin publishes his Origin of Species and uses the “tree of life” metaphor in Chap. 4. The book contains a hypothetical branching diagram that illustrates how species gradually diverge through time by means of natural selection

1861:

Heinrich Anton de Bary identifies microorganisms as the cause of plant diseases, and he later introduces the concept of symbiosis

1866:

Gregor Mendel introduces his laws of inheritance

1866:

Ernst Haeckel introduces the first non-hypothetical “Tree of Life”

1868:

Johannes Friedrich Miesher names a substance inside the nucleus of cells “nuclein” (DNA)

1870:

Thomas Henry Huxley distinguishes biogenesis from abiogenesis and denies abiogenesis (alternatively known as spontaneous generation)

1873/1875:

Pierre Joseph van Beneden identifies parasitic microorganisms as the cause of animal diseases and distinguishes between commensalism, parasitism, and mutualism

1875:

Ferdinand Cohn introduces a first classification of bacteria

1876:

Robert Koch identifies the Anthrax bacillus responsible for “Milzbrand-Krankheit” (anthrax disease) and proves earlier theoretical versions of the germ theory of disease to be true

1877:

Paul Ehrlich starts his career by developing new techniques to color bacteria. These techniques will enable him to specify the various types of blood cells there exist, research that will found the study of both serology and immunology

1878:

Louis Pasteur’s work on the germ theory of disease is read before the French Academy of Sciences

1879:

Timothy Lewis identifies microorganisms inside the bloodstream of humans and links them to disease

1880:

Charles Louis Alphonse Laveran identifies flagella-like motile unicellular organisms that he identifies as causal agents of malaria

1882:

Ilya Ilyich Mechnikov observes what he later calls phagocytosis: cell eating. Phagocytosis is crucial to understand immunity as well as primary, secondary, and tertiary symbiosis

1884:

Robert Koch publishes his etiology of tuberculosis that proves that the tubercle bacillus is the disease-causing agent of tuberculosis

1884:

Hans Christian Joachim Gram develops the Gram stain technique that enables to differentiate between “gram-negative” and “gram-positive” bacteria

1885:

Auguste Weismann develops his “transmutation hypothesis.” The work is foundational for the “Weismann barrier” that puts a halt to (neo-)Lamarckian theories

1886:

Theodor Escherich identifies a “bacterium coli commune” that resides in the human gut (E. coli)

1886:

D.E. Salmon and Theobald Smith improve vaccination therapies by injecting whole heat-killed cells of virulent strains

1886:

Adolf Mayer describes the tobacco mosaic disease

1888:

The Pasteur Institute is founded in France

1890:

The Cold Spring Harbor Laboratory is founded in Brooklyn, New York

1891:

The Robert Koch Institute is founded in Germany

1891:

Paul Ehrlich discovers antibodies

1892:

Dmitri Iwanowski demonstrates that the tobacco mosaic disease is caused by a non-bacterial infectious agent

1898:

Martinus Beijerinck defines the agent responsible for the tobacco mosaic disease as a virus which he characterizes as a “living and fluid infectious agent”

1900:

Mendel’s hereditary laws are (re)discovered by Hugo de Vries, Carl Correns, and Erich von Tschermak

1902/1910:

Fred Neufeld classifies Pneumococci into three different types

1905:

Constantin Mehrezkowsky introduces a double-origin theory of life, a view he illustrates with a reticulate “tree of life” in 1910

1909:

Theodor Boveri and Walter Sutton introduce the chromosome theory

1909:

Wilhelm Johannsen distinguishes between the genotype and phenotype

1912:

Friedrich Karl von Faber introduces the notion of “erbliche Zusammenleben” (hereditary symbiosis)

1915:

Hermann Reinheimer introduces the metaphor of the “web of life”

1915:

Frederick Twort discovers bacterial lysis and assumes it is induced by viral agents that infect bacteria

1917:

Félix d’Herelle cultures viruses that infect bacteria and calls them “bacteriophages”

1928:

Frederick Griffith reports on bacterial transformation

1929:

Alexander Fleming reports that the mold Penicillium notatum undertakes “antibacterial action” against gram-positive microorganisms

1931:

Ernst Ruska and Max Knoll build the first electron microscopes

1932:

Julius Petrie introduces serological typing

1938:

Warren Weaver coins the term “molecular biology”

1941:

George Beadle and Edward Tatum demonstrate that protein synthesis as well as the function of enzymes is controlled by genes and they introduce the “one gene–one enzyme theory” (a term coined by Norman Horowitz)

1942:

Conrad Waddington coins the term “epigenetics”

1942:

Julian Huxley characterizes the late nineteenth century as the “eclipse of Darwinism”

1943:

Salvador Luria and Max Delbrück demonstrate that bacteria evolve according to Darwinian principles (they “mutate” randomly)

1944:

Oswald Avery, Colin MacLeod, and Maclyn McCarthy confirm that bacteria can transform and they identify DNA as the transforming principle

1944:

Barbra McClintock discovers “jumping genes,” what we now call “transposons” or “mobile genetic elements” in maize

1944:

Albert Schatz isolates the antibiotic streptomycin from Streptomyces griseus at Selman Waksman’s laboratory which becomes administered against tuberculosis

1946:

Joshua Lederberg and Edward Tatum report on bacterial conjugation in the E. coli K-12 strain

1950/1953:

André Lwoff and Antoinette Gutmann distinguish between the lysogenic and lytic phases of bacteriophages and introduce the concept of “prophage”

1950:

Antibiotics such as streptomycin, penicillin, and chloramphenicol are massively produced and administered

1951:

Victor Freeman reports on HGT from a bacteriophage to C. diphtheria

1951:

Esther Lederberg discovers that E. coli can become infected with a bacteriophage that she calls lambda

1952:

Joshua Lederberg, Luigi-Luca Cavalli Sforza, and Esther Lederberg, and independently William Hayes, report on the Fertility factor in E. coli that enables bacterial conjugation

1952:

Norton Zinder and Joshua Lederberg report on phage-mediated bacterial transduction

1952:

Joshua Lederberg introduces the plasmid concept to designate all extrachromosomal DNA by which he intends to include mitochondrial and chloroplast DNA (still a theoretical notion) and viral prophages, and he applies the notion of “hereditary symbiosis” as well as “infective heredity” to the phenomena of bacterial transformation, phage-mediated transduction, and bacterial conjugation

1952:

Alfred Hershey and Martha Chase perform the Hershey–Chase experiments with bacteriophage T2 and the E. coli bacterium and confirm that DNA, and not proteins, carries hereditary information

1953:

X-ray crystallography of DNA performed by Rosalind Franklin leads Francis Crick, Maurice Wilkins, and James Watson to describe the double-helical structure of DNA

1955:

Norton Zinder demonstrates transduction of antibiotic resistance genes

1959–1963:

Japanese scholars Kunitaro Ochia, Tomoichiro Akiba, and Tsutomu Watanabe report on bacteria that have acquired resistance genes against antibiotics in natural settings and identify bacterial conjugation as the likely mode of transfer

1959:

Arthur Pardee, François Jacob, and Jacques Monod (1959) publish the “PaJaMo” paper that demonstrates protein regulation of gene expression, or gene regulatory networks. They base their work on their studies of galactosidase fermentation in E. coli

1963:

Linus Pauling and Émile Zuckerkandl map the changes in hemoglobin polypeptide chains of different mammalian species and find that “semantides”: “DNA, RNA, and polypeptides” lend themselves for comparative bimolecular analysis

1969/1970:

Stanley Cohen, Annie Chang, and Leslie Hsu demonstrate that E. coli can take up plasmids carrying antibiotic resistance genes (R factors)

1970:

Howard Temin and S. Mizutani, and independently David Baltimore, discover reverse transcriptase

1972:

Susumo Ohno introduces the concept of “Junk DNA”

1976:

Richard Dawkins introduces the “selfish gene” theory

1977:

Frederic Sanger sequences the first entire genome of a bacteriophage

1977:

Carl Woese and George Fox divide prokaryotes into Archaebacteria and Eubacteria which they define as “urkingdoms” or “primary kingdoms”

1977:

Bukharo, Shapiro, and Adhya identify insertion sequences

1977:

Shine and colleagues identify long terminal repeats (LTRs) in the genome of the avian sarcoma virus

1977:

Allan Campbell and colleagues provide a first nomenclature of transposable elements in prokaryotes

1978:

Whittaker and Margulis introduce a 5-kingdom classification of life that understands symbiogenesis as the defining mechanism that separates prokaryotes (Monera) from all 4 eukaryotic kingdoms, and in subsequent years, Margulis introduces new, reticulate evolutionary iconography

1979:

Variola is declared eradicated

1979:

James Shapiro describes the RNA intermediate stage of retrotransposons

1979:

Yen, Hu, and Marrs (1979, Marrs 1974) report on “nucleoprotein particles that act as vectors of genetic exchange,” i.e., GTAs in Rhodopseudomonas capsulata (today called Rhodobacter capsulatus)

1980:

Alex Champion uses the concepts of “HGT” and “reticulate evolution” to understand the evolution of Pseudomonas fluorescens

1981:

Joachim Messing develops the shotgun DNA sequencing technique which enables the sequencing of longer stretches of DNA up to whole genomes

1981:

Esther Lederberg provides a classification system for insertion sequences

1982:

Maxine Singer distinguishes between Short Interspersed Nuclear Elements (SINEs) and Long Interspersed Nuclear Elements (LINEs)

1983:

Kary Mullis introduces the polymerase chain reaction (PCR) technique

1983:

James Shapiro edits a first anthology on “mobile genetic elements”

1984:

Michael Syvänen introduces the notion of “cross-species gene exchange”

1989:

Peter Gogarten and colleagues introduce ATPase-based phylogenetic reconstructions of the roots of the tree of life and suggest that these genes were acquired by “HGT”

1989:

Jack Heinemann and George Sprague demonstrate that “Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast (Saccharomyces cerevisiae)”

1989:

The American Society for Microbiology publishes their first anthology on mobile DNA, the work is edited by Douglas Berg and Martha Howe

1989:

Douglas Berg and Martha Howe differentiate between compositional and non-compositional insertion sequences

1989:

Stokes and Hall differentiate integrons as “a novel family of potentially mobile DNA elements encoding site-specific gene integration functions”

1990:

Hacker and coworkers introduce the concept of pathogenicity islands to designate specific regions in the genome of bacterial pathogens that are absent in non-pathogenic bacteria

1990:

Woese, Kandler, and Wheelis introduce the three-domain classification of life (Archaea, Bacteria, and Eukaryota)

1994:

The Tree of Life Web Project (ToL) commences and goes online in 1996

1995:

The complete genome of Haemophilus influenza is sequenced by Craig Venter, Hamilton O. Smith, and Claire Fraser at the Institute for Genomic Research

1998:

Didier Mazel and colleagues discover superintegrons in Vibrio cholerae bacteria

1998:

Jo Handelsman and colleagues introduce the term “metagenomics” to designate biochemical techniques used to identify the genetic constitution of unidentified soil bacteria

1999:

Ford W. Doolittle introduces a hypothetical reticulate image and the metaphor of a “web of life” to visualize and conceptualize the massive HGT that occurs across all three domains of life

1999:

Eisterling and colleagues report on a “bacteriophage-like particle,” the “voltae transfer agent,” of Methanococcus voltae PS. This GTA enables transductions between members of the bacterial strain

2000:

Andrew S. Lang and J.T. Beatty report on a GTA in the purple non-sulfur bacterium Rhodobacter capsulatus

2000:

Peter Gogarten introduces the metaphor of a “net” and “network” of life

2001/2002:

The American National Science Foundation launches the AToL—Assembling the Tree of Life Project

2002:

The American Society for Microbiology publishes their second anthology on mobile DNA, which is edited by Nancy L. Craig, Robert Craigie, Martin Gellert, and Alan M. Lambowitz

2003:

The barcoding technique is introduced by Paul Hebert and colleagues

2004:

Maria Rivera and James Lake introduce the “ring of life”

2004:

The American Journal of Botany dedicated a special issue to the tree of life of plants

2005:

In an article for Scientific American, Ford Doolittle expands his reticulate evolutionary image in order to include the symbiogenetic acquisition of chloroplasts and mitochondria

2005:

Fan Ge, Li-San Wang, and Junhyong Kim introduce the metaphor of a “cobweb” of life

2005:

The Tree Thinking Group goes online

2006:

Bork’s team publishes their circular tree of life (Ciccarelli et al. 2006) in Science and launches the online iTOL project

2009:

The New Scientist features a reticulate tree of life image on their January 21st cover and titles it “Darwin was wrong: Cutting down the tree of life.” Daniel Dennett, Jerry Coyne, Richard Dawkins, and Paul Meyers argue that the cover feeds into creationism

2009:

Tal Dagan and William Martin introduce networks that depict actual horizontal as well as vertical exchange between distinct microbial lineages

2009:

The Philosophical Transactions of the Royal Society, B: Biological Sciences features a theme issue on “The network of life: genome beginnings and evolution”

2010:

Luis Villarreal and Günter Witzany introduce a hypothetical diagram that illustrates the viral origin of life as well as the colonization of all three domains of life by viral agents

2010:

The journal Biology and Philosophy features a special issue on the tree of life

2011:

The journal Research in Microbiology dedicates a special issue to “Archaea and the tree of life”

2011:

Biology Direct publishes an issue titled “Beyond the Tree of Life”

2014:

The American National Science Foundation launches the GoLife (Genealogy of Life) project

2014:

The Journal of Ecology features a special issue on “The tree of life in ecosystems: evolution of plant effects on carbon and nutrient cycling”

Note: This timeline is based upon the timeline provided by the American Society for Microbiology (ASM) available at http://www.asm.org/index.php/choma3/71-membership/archives/7852-significant-events-in-microbiology-since-1861; the Genome News Network site at http://www.genomenewsnetwork.org/resources/timeline; as well as own work.