Molecular Biology and Pathogenicity of Mycoplasmas
Abstract
The recent sequencing of the entire genomes of Mycoplasma genitalium and M. pneumoniae has attracted considerable attention to the molecular biology of mycoplasmas, the smallest self-replicating organisms. It appears that we are now much closer to the goal of defining, in molecular terms, the entire machinery of a self-replicating cell. Comparative genomics based on comparison of the genomic makeup of mycoplasmal genomes with those of other bacteria, has opened new ways of looking at the evolutionary history of the mycoplasmas. There is now solid genetic support for the hypothesis that mycoplasmas have evolved as a branch of gram-positive bacteria by a process of reductive evolution. During this process, the mycoplasmas lost considerable portions of their ancestors’ chromosomes but retained the genes essential for life. Thus, the mycoplasmal genomes carry a high percentage of conserved genes, greatly facilitating gene annotation. The significant genome compaction that occurred in mycoplasmas was made possible by adopting a parasitic mode of life. The supply of nutrients from their hosts apparently enabled mycoplasmas to lose, during evolution, the genes for many assimilative processes. During their evolution and adaptation to a parasitic mode of life, the mycoplasmas have developed various genetic systems providing a highly plastic set of variable surface proteins to evade the host immune system. The uniqueness of the mycoplasmal systems is manifested by the presence of highly mutable modules combined with an ability to expand the antigenic repertoire by generating structural alternatives, all compressed into limited genomic sequences. In the absence of a cell wall and a periplasmic space, the majority of surface variable antigens in mycoplasmas are lipoproteins. Apart from providing specific antimycoplasmal defense, the host immune system is also involved in the development of pathogenic lesions and exacerbation of mycoplasma induced diseases. Mycoplasmas are able to stimulate as well as suppress lymphocytes in a nonspecific, polyclonal manner, both in vitro and in vivo. As well as to affecting various subsets of lymphocytes, mycoplasmas and mycoplasma-derived cell components modulate the activities of monocytes/macrophages and NK cells and trigger the production of a wide variety of up-regulating and down-regulating cytokines and chemokines. Mycoplasma-mediated secretion of proinflammatory cytokines, such as tumor necrosis factor alpha, interleukin-1 (IL-1), and IL-6, by macrophages and of up-regulating cytokines by mitogenically stimulated lymphocytes plays a major role in mycoplasma-induced immune system modulation and inflammatory responses.
“Life is extremely conservative. On whatever level—the individual organism, the species, the biota as a whole—life expends energy such that it preserves its past, even if, paradoxically, various threats force it to innovate.”
Lynn Margulis and Dorion Sagan (279a)
The recent sequencing of the entire genomes of Mycoplasma genitalium (139) and M. pneumoniae (181) has attracted considerable attention among life scientists to the molecular biology of mycoplasmas, the smallest self-replicating organisms. It appears that we are now much closer to the goal of defining, in molecular terms, the entire machinery of a self-replicating cell. Considerable advances were also made toward a better understanding of mycoplasma pathogenesis. Most impressive are the findings concerning the interaction of mycoplasmas with the immune system, macrophage activation, cytokine induction, mycoplasma cell components acting as superantigens, and autoimmune manifestations. Evasion of the host immune system by antigenic variation of mycoplasmal surface components, as well as molecular definition of mycoplasmal adhesins, has also gained much attention recently. The demonstration of the ability of mycoplasmas to enter host cells and the possibility that several human mycoplasmas act as accessory factors in the activation of AIDS played a role in intensifying research on mycoplasma pathogenesis, bringing more researchers into the circle of those interested in this group of organisms. We were thus prompted to try and summarize within the framework of a single comprehensive review the cell biology and pathogenicity of the mycoplasmas, emphasizing when possible the lessons that can be learned from the mycoplasmal genome projects on the minimal complement of genes enabling life.
Mycoplasmas are distinguished phenotypically from other bacteria by their minute size and total lack of a cell wall. Taxonomically, the lack of cell walls is used to separate mycoplasmas from other bacteria in a class named Mollicutes (mollis, soft; cutis, skin, in Latin). The current classification of Mollicutes and the properties distinguishing the currently established taxa are presented in Table Table1.1. While the trivial terms “mycoplasmas” or “mollicutes” have been used interchangeably to denote any species included in Mollicutes, the trivial names ureaplasmas, entomoplasmas, mesoplasmas, spiroplasmas, acholeplasmas, asteroleplasmas, and anaeroplasmas are routinely used for members of the corresponding genera. The preliminary molecular characterization of the uncultured plant and insect mycoplasma-like organisms (MLOs) has provided strong experimental support for their inclusion in the class Mollicutes. Consequently, the trivial term “phytoplasmas” has been proposed to replace the awkward name “mycoplasma-like organisms.”
TABLE 1
Major characteristics and taxonomy of the class Mollicutesa
Classification | Current no. of recognized species | Genome size (kb) | Mol% G+C of genome | Cholesterol requirement | Distinctive properties | Habitat |
---|---|---|---|---|---|---|
Order I: Mycoplasmatales | ||||||
Family I: Mycoplasmataceae | ||||||
Genus I: Mycoplasma | 102 | 580–1,350 | 23–40 | Yes | Optimum growth at 37°C | Humans, animals |
Genus II: Ureaplasma | 6 | 760–1,170 | 27–30 | Yes | Urea hydrolysis | Humans, animals |
Order II: Entomoplasmatales | ||||||
Family I: Entomoplasmataceae | ||||||
Genus I: Entomoplasma | 5 | 790–1,140 | 27–29 | Yes | Optimum growth at 30°C | Insects, plants |
Genus II: Mesoplasma | 12 | 870–1,100 | 27–30 | No | Optimum growth at 30°C; 0.04% Tween 80 required in serum-free medium | Insects, plants |
Family II: Spiroplasmataceae | ||||||
Genus I: Spiroplasma | 33 | 780–2,220 | 24–31 | Yes | Helical motile filaments; optimum growth at 30–37°C | Insects, plants |
Order III Acholeplasmatales | ||||||
Family I: Acholeplasmataceae | ||||||
Genus: Acholeplasma | 13 | 1,500–1,650 | 26–36 | No | Optimum growth at 30–37°C | Animals, some plants, insects |
Order IV: Anaeroplasmatales | ||||||
Family: Anaeroplasmataceae | ||||||
Genus I: Anaeroplasma | 4 | 1,500–1,600 | 29–34 | Yes | Oxygen-sensitive anaerobes | Bovine/ovine rumen |
Genus II: Asteroleplasma | 1 | 1,500 | 40 | No | Oxygen-sensitive anaerobes | Bovine/ovine rumen |
Undefined taxonomic status | ||||||
Phytoplasma | NDb | 640–1,185 | 23–29 | Not known | Uncultured in vitro | Insects, plants |
Because of the wide scope of the review and space limitations, emphasis will be put on the more recent findings, published since 1990. The interested reader is referred to a number of books on various aspects of mycoplasmology published during the last decade or so (210, 277, 365, 370, 395, 459, 473). A wealth of information can be found in the proceedings of the biannual meetings of the International Organization for Mycoplasmology (the last issues were named IOM Letters, volumes 1 through 4), and in a special issue of Journal of Clinical infectious Diseases (volume 17, supplement 1, 1993). Reviews covering different aspects of the molecular biology and genetics of mycoplasmas, as well as their general properties and taxonomy, are also available (30, 56, 111, 114, 356, 357, 359–361).
ACKNOWLEDGMENTS
We thank Richard Herrmann, Ruth Gallily, and Dennis J. Pollack for critical reading of the manuscript. Their comments and suggestions are greatly appreciated.
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