2983 Spiroplasmas: Evolutionary Relationships and Biodiversity Laura B. Regassa 1 and Gail E. Gasparich 2
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[Frontiers in Bioscience 11, 2983-3002, September 1, 2006] Spiroplasmas: evolutionary relationships and biodiversity Laura B. Regassa 1 and Gail E. Gasparich 2 1 Department of Biology, Georgia Southern University, PO Box 8042, Statesboro, GA 30460 and 2 Department of Biological Sciences, Towson University, 8000 York Road, Towson, MD 21252 TABLE OF CONTENTS 1. Abstract 2. Introduction 3. Spiroplasma Systematics 3.1. Taxonomy 3.1.1. Spiroplasma species concept 3.1.2. Current requirements for classification of Spiroplasma species 3.1.3. Polyphasic taxonomy 3.2. Molecular Phylogeny 3.2.1. Evolutionary relationship of spiroplasmas to other Eubacteria 3.2.2. Evolutionary relationships within the genus Spiroplasma 3.2.2.1. The Ixodetis clade 3.2.2.2. The Citri-Chrysopicola-Mirum clade 3.2.2.3. The Apis clade 3.2.2.4. The Mycoides-Entomoplasmataceae clade 3.2.3. Comparative genomics 4. Biodiversity 4.1. Host Range and Interactions 4.1.1. Insect pathogens 4.1.2. Plant pathogens 4.1.3. Higher order invertebrate pathogens 4.1.4. Vertebrate pathogenicity 4.2. Host Specificity 4.3. Biogeography 5. Perspectives 6. Acknowledgments 7. References 1. ABSTRACT Spiroplasmas are wall-less descendants of Gram- 34 groups based on cross-reactivity of surface antigens. positive bacteria that maintain some of the smallest Three of the serogroups contain closely related strain genomes known for self-replicating organisms. These complexes that are further divided into subgroups. helical, motile prokaryotes exploit numerous habitats, but Phylogenetic reconstructions based on 16S rDNA are most often found in association with insects. Co- sequence strongly support the closely related evolution with their insect hosts may account for the highly serogroups. To date, less than 40 Spiroplasma species speciose nature of the genus Spiroplasma, with many have been fully characterized and given binomial names. spiroplasmas existing in obligate insect/plant transmission Complete characterization of a new species involves cycles. In addition to insect and plant hosts, spiroplasmas numerous phenotypic and genotypic tests as outlined in are found in association with ticks and crustaceans. the minimal standards document; this document is Although most spiroplasma associations appear to be currently under revision to include phylogenetic data commensal, some cases of pathogenicity or mutualism have and a reevaluated set of required phenotypic and been described. Most notably, spiroplasmas have been genotypic tests. The area of spiroplasma research is identified as the causative agents of agricultural and poised for major advances with new criteria for naming aquacultural diseases and the sex ratio disorder in insects. species in preparation, a dramatic increase in available Some spiroplasmas exhibit strict host and/or geographical molecular characters, the promise of full genome ranges, but others are relative generalists. Species of the sequences, and advances in genetic tools for genus Spiroplasma have been traditionally classified into manipulation of these organisms. 2983 Spiroplasmas: Evolution and Biodiversity 2. INTRODUCTION 3. SPIROPLASMA SYSTEMATICS Spiroplasmas are among the smallest self- 3.1. Taxonomy replicating prokaryotes known, with genomes ranging in The taxonomic requirements for naming new size from approximately 780-2,220 kbp (1,2). They are spiroplasma species are governed by the 1995 guidelines helical, motile bacteria that apparently evolved via published by the International Committee on Systematic simplification of Gram-positive bacteria, although they lack Bacteriology (ICSB) Subcommittee on Taxonomy of a cell wall (3,4). As the organisms radiated to occupy Mollicutes (36); this committee has since been renamed the multiple habitats, they became able to invade the arthropod International Committee on Systematics of Prokaryotes gut lumen. Some species expanded their habitat range to (ICSP). The 1995 guidelines are revisions of earlier include arthropod hemolymph, ovaries, fat bodies, documents outlining the minimal standards for description hypodermis, and salivary glands. With much lower of Mycoplasma species. The first document providing frequency spiroplasmas have also been found in association general guidelines for naming species of Mycoplasmatales with ticks, plants and higher order invertebrates (5-11). was published in 1967 by the ICSB Subcommittee on the Most spiroplasmas appear to be commensals, but there are Taxonomy of Mycoplasmatales (37) In 1972, a few cases of mutualism or pathogenicity associated with modifications to the original document resulted in spiroplasma infections (12,13,14). publication of the minimal standards for description of mycoplasma species (38); this document was then revised Although insects are the main reservoir for in 1979 and 1995. The revisions reflect changes in spiroplasmas (15), other early isolations were made from Mollicutes systematics over time, and there is currently a secondary hosts that were adversely affected by movement within Mollicutes systematics to introduce spiroplasma infections. Description of the genus another revision to the classification system. The ICSP Spiroplasma began with the isolation and characterization Subcommittee on Taxonomy of Mollicutes reported that a of the causative agent of citrus stubborn disease (16), S. newly revised minimal standards document for description citri (17). S. citri infects the plant phloem sieve tubes, with of Mycoplasma species was being drafted (ICSP the pathogenic spiroplasma being delivered to the plants via Subcommittee, 11 July 2004 meeting, Athens Georgia; R. sap-feeding insects. The infected sieve elements then serve F. Whitcomb, personal communication). This section will as a reservoir for transmission to other sap-feeding insects review the current requirements for Spiroplasma species (reviewed in 18). The second described member of the designation and discuss some of the issues that have led to genus Spiroplasma, S. kunkelii, causes corn stunt disease a call to revise the criteria. and also resides in an obligate cyclical habitat that consists of both plant phloem and an insect vector (19-21). Another 3.1.1. Spiroplasma species concept early member of the genus Spiroplasma was the previously Although the species is the basal category for described microorganism that causes a sex-ratio taxonomic classification, the definition of a bacterial species is abnormality in Drosophila; it was originally thought to be a relatively vague and artificial (39,40). Nature often represents spirochaete but was later identified as a spiroplasma and a continuum rather than discrete points, such as clearly named S. poulsonii (22-24). Spiroplasmas were also differentiated species (41). As more and more spiroplasmas isolated from ticks (25-29). One of the tick isolates, S. are isolated and characterized, the continuous nature of mirum, is referred to as the suckling mouse cataract agent spiroplasma biodiversity, at least in some serogroups, is due to its ability to establish experimental infections and becoming clear. For example, the group VIII strains once disease in suckling mice (27,28,30-32). As research on represented several clearly defined species but are now a huge spiroplasmas proceeded and more isolates were collection of inter-related strains that cannot be clearly defined characterized, it became apparent that insects served as the using the current criteria (42,43). major reservoir for spiroplasma maintenance and dispersal (14,15), and that plant surfaces were more important in The basic species concept for Spiroplasma is rooted dispersal and transmission than the plant phloem (33-35). in the species concept for other prokaryotic taxa (44,45), which requires genomes exhibiting less than 70% similarity for This early work on spiroplasmas led to the separate species designations (46,47). In theory, this development of methods for cultivation and requirement was satisfied by completing DNA-DNA characterization, resulting in a proliferation of spiroplasma reassociation analyses; the limited reassociation data that was isolates from varied hosts and diverse geographical locales. generated was found to be consistently complementary to the To date, 36 Spiroplasma species have been completely analysis of surface antigens (48-52). These comparisons described and given binomial names. Hundreds of other validated the use of serological analyses as the basis for isolates have been partially described, and some of these Spiroplasma species designations (36). A detailed historical undoubtedly represent new Spiroplasma species. The wide review on the movement toward a serological classification range of hosts and geographic distribution offers some system was recently provided by Gasparich (53). challenges for thoroughly describing this genus, but it also provides some interesting opportunities to explore 3.1.2. Current requirements for classification of questions of biodiversity, co-evolution and phylogenetic Spiroplasma species relationships. This article will explore the areas of The current minimal standards for spiroplasma spiroplasma biodiversity and their evolutionary species designation rely upon phenotypic and genotypic relationships. information. As described by the ICSB Subcommittee on 2984 Spiroplasmas: Evolution and Biodiversity Taxonomy of Mollicutes, an isolate must be examined for (e.g. S. floricola (70), S. gladiatoris (71)). The range of morphology and serology as well as molecular and temperatures for growth, including the optimal