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[Frontiers in Bioscience 7, D1762-1781, August 1, 2002] 1762 the NECESSITY of COMBINING GENOMIC and ENZYMATIC DATA to INFER META

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[Frontiers in Bioscience 7, D1762-1781, August 1, 2002] 1762 the NECESSITY of COMBINING GENOMIC and ENZYMATIC DATA to INFER META [Frontiers in Bioscience 7, d1762-1781, August 1, 2002] THE NECESSITY OF COMBINING GENOMIC AND ENZYMATIC DATA TO INFER METABOLIC FUNCTION AND PATHWAYS IN THE SMALLEST BACTERIA: AMINO ACID, PURINE AND PYRIMIDINE METABOLISM IN MOLLICUTES J. Dennis Pollack Department of Molecular Virology, Immunology and Medical Genetics, The College of Medicine and Public Health, The Ohio State University, 333 West 10th Avenue, Columbus, OH 43210 TABLE OF CONTENTS 1. Abstract 2. Introduction 3. Metabolic Linkages to Amino Acids and Proteins 4. Amino Acids: Transport 5. Amino Acids: Biosynthesis and Metabolism 6. Amino Acids: Aromatic amino acid synthesis in Acholeplasma-Anaeroplasma 7. Purine Metabolism: Transport 8. Purine Metabolism: Interconversions 9. Purine Metabolism: Intervention of the pentose phosphate pathway and glycolysis 10. Purine Metabolism: Metabolic consensus 11. Pyrimidine Metabolism: Interconversions and metabolic consensus 12. Predicting Metabolism 13. Acknowledgements 14. References 1. ABSTRACT Bacteria of the class Mollicutes have no cell wall. represent these simple microbes. Mycoplasma genitalium, a One species, Mycoplasma genitalium is the personification Mollicutes with a genome of 580 kbp and 475 ORFs, has of the simplest form of independent cell-free life. Its small the smallest genome in any free-living cell and is an genome (580 kbp) is the smallest of any cell. Mollicutes obvious example of the simplest organism. It is the minimal have unique metabolic properties, perhaps because of their cell and defines-characterizes, personifies independent limited coding space and high mutability. Based on 16S cellular life. rRNA analyses the Mollicutes Mycoplasma gallisepticum is thought to be the most mutable Bacteria. Enzyme activities All Mollicutes, like M. genitalium have no cell found in most Bacteria are absent from Mollicutes. The wall, are small, passing through 0.45 mµ porosity filters. functions of apparently absent genes and enzymes can Some have a cholesterol growth requirement, most have a apparently be fulfilled by other genes and their expression low 24-33% G+C, they have 1-2 rRNA operons, their 5S products that have multiple capabilities. Because of these rRNAs have 104-113 nucleotides and some use the UGA and other properties predictions of their metabolism based “universal” stop codon as a tryptophan codon. Their RNA only on, e.g., either annotation, enzymatic assay, proteomic polymerase is rifampicin resistant; they lack cytochromes studies or structural analyses is problematic. To obtain a and the tricarboxylic acid cycle. Unlike other bacteria, more confident appraisal of the functional capabilities of some Mollicutes genera have NADH oxidase activity these simplest cells genomic and enzymatic data were localized in their cytoplasm, some genera do not possess combined to obtain a “metabolic consensus”. The the “ubiquitous” DNA repair enzyme uracil-DNA consensus is represented by a biochemical circuit for glycosylase. Some Mollicutes can transport nucleoside central metabolism involving purine and pyrimidine monophosphates or have an obligate requirement for interconversions and their linkages to amino acid pyrophosphate rather than ATP for glycolysis or the metabolism, glycolysis and the pentose phosphate pathway phosphorylation of nucleosides. The “household” in three human Mollicutes pathogens: Mycoplasma nucleoside diphosphate kinase (NDPK) gene is not pneumoniae, Mycoplasma genitalium and Ureaplasma annotated in the four Mollicutes whose genomes are urealyticum. sequenced; NDPK activity was not found in Mycoplasma pneumoniae. 2. INTRODUCTION Mollicutes have been frequently reported as In a search for a metabolic model of independent “unrecognized” contaminants in a large number of life the simplest microbes were seen as the most profitable established cell lines, and they confound much research examples to study. The bacteria in the class Mollicutes because of such intimacy. They infect and cause a 1762 Combinatorial Genomics in Mollicutes (Mycoplasmas) frequently encountered treatable low-mortality respiratory chemically defined or semi-defined growth media. disease of humans. In the U. S. and abroad, they cause Unfortunately, there have been few successes and scant enormous economic losses as subtle or severe pathogens of continued study. The circumstances are most probably cattle, swine, sheep, goats and poultry. Treatment of large related to the expense of producing large quantities of such numbers of infected animals or birds by antibiotics is media and the relatively poor growth yields of some of the infrequent, sacrifice of the exposed herd or flocks is a putatively more “interesting” organisms, i.e., the human preventative solution. Mollicutes also cause commercial pathogens: M. pneumoniae, M. genitalium and U. losses as pathogens of corn and citrus; their infection of urealyticum. pollinating bees has a high mortality. They are ubiquitous and some are capable of an intracellular existence; they are Smith (123) and Rodwell (109-111) and Miles relatively difficult to eradicate from host tissues. (74) in their reviews, among others, on the nutrition of the Mollicutes described a synthetic medium (Medium E) for To understand Mollicutes more fully, we have M. mycoides, strain Y, lacking protein, e.g., containing no studied their metabolism in cell-free culture (100). This BSA or casein digests. Tourtellotte et al. developed a review continues and expands upon that report but synthetic medium for Acholeplasma. laidlawii B described emphasizes Mollicutes amino acid, purine, pyrimidine in reference 110. Synthetic media for Spiroplasma spp. biochemistry; it primarily correlates enzymatic activity and (20,48) and Anaeroplasma intermedium (Medium D, with gene annotations in order to obtain a more complete picture amino acids, vitamins, and phosphatidylcholine) have also of their metabolism that could be derived from either data been reported (108). base alone. In this manner, a “consensus metabolism” is presented here for the first time. A companion and earlier Metabolic studies are complicated by the article have dealt predominantly with Mollicutes necessary culture of Mollicutes in undefined complex- carbohydrate metabolism and their respiration (92,100). protein rich media (references are cited in 35,73,110). The complications involve the incompletely defined nutritional We believe that the study of Mollicutes needs of the organism and the less appreciated possibility metabolism requires the combination of enzymatic, that some “too-rich” media formulations are inimical to annotation, gene expression and structural data. The optimal growth. Gardella and DelGuidice and others “combinatorial” approach serves two purposes: 1) it emphasized that some Mollicutes are sensitive to inhibitors validates putative and individual observations that may be present in conventional protein-yeast-serum rich Mollicutes derived from only one data base, i.e., they are mutually media (43,119). supportive. This occurs, for example, when a gene (Gene C) is annotated in an otherwise recognized metabolic The reported amino acid requirements for the sequence known to contain say 5 components, A, B, C, D growth of various Mollicutes have been listed in detail (35). and E. In this scenario, enzymatic assays had demonstrated Other studies document the role of Mollicutes proteases the presence of components A and E. Combining the data that cleave growth medium proteins to small peptides and suggests more strongly that the entire pathway is present amino acids that then become available for transport and functional. 2) Further, the reliability or confidence in (1,19,120,137). Miles has reviewed protease activities the annotation of Gene C itself is improved by virtue of the reported in Mollicutes (75). Various peptidase activities fact that the metabolically linked activities or their genes possibly related to arthritic disease were reviewed by (i.e., A and E) are also known. Gabridge et al. (38). Various proteases and peptidases have been putatively annotated in M. pneumoniae, M. In order to compensate for an apparently limited genitalium, M. pulmonis and U. urealyticum coding capacity and the absence of “essential (18,26,37,45,50). Regula et al. (107) identified a protease housekeeping” enzymes, e.g., nucleoside diphosphate in proteomic expression studies of M. pneumoniae. kinase (NDPK), Mollicutes have a number non-specific enzymatic activities (glycolytic kinases) that apparently 4. AMINO ACIDS: TRANSPORT replace some or all of the missing functions of NDPK (96). Such “genomic economy” in a small genome may spare Genomic or enzymatic evidence of amino acid both any coding restraint and the elaboration of additional transport or synthesis in Mollicutes is limited. The apparent proteins. Genomic economy of another sort is represented absence of genes for the synthesis of amino acids suggested by the apparent presence of a multienzyme (single) protein that there would be a large number of transporters, but such that can carry out more than one enzymatic function, i.e., expectations in M. genitalium and M. pneumoniae were not the lactate/malate dehydrogenase (LDH/MDH) protein of confirmed by annotation, although histidine, glutamine, Mycoplasma spp. (23,24,92). These observations and oligopeptide and general amino acid permease transporters hypotheses are cautionary in relation to the reliability and were annotated (37,50). In M. pulmonis, there is an accuracy of enzymatic or metabolic predictions (90). annotated arginine-ornithine
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