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Proc Natl Acad Sci U S A. 2005 May 17; 102(20): 7309–7314. Published online 2005 May 9. doi: 10.1073/pnas.0502314102. | PMCID: PMC1129125 |
Copyright © 2005, The National Academy of Sciences Microbiology Genomic and proteomic comparisons between bacterial and archaeal genomes and related comparisons with the yeast and fly genomes Samuel Karlin,*† Luciano Brocchieri,* Allan Campbell,‡ Martha Cyert,‡ and Jan Mrázek* Departments of *Mathematics and ‡Biological Sciences, Stanford University, Stanford, CA 94305-2125 Bacterial, archaeal, yeast, and fly genomes are compared with respect to predicted highly expressed (PHX) genes and several genomic properties. There is a striking difference in the status of PHX ribosomal protein (RP) genes where the archaeal genome generally encodes more RP genes and fewer PHX RPs compared with bacterial genomes. The increase in RPs in archaea and eukaryotes compared with that in bacteria may reflect a more complex set of interactions in archaea and eukaryotes in regulating translation, e.g., differences in structure requiring scaffolding of longer rRNA molecules, expanded interactions with the chaperone machinery, and, in eukaryotic interactions with endoplasmic reticulum components. The yeast genome is similar to fast-growing bacteria in PHX genes but also features several cytoskeletal genes, including actin and tropomyosin, and several signal transduction regulatory proteins from the 14.3.3 family. The most PHX genes of Drosophila encode cytoskeletal and exoskeletal proteins. We found that the preference of a microorganism for an anaerobic metabolism correlates with the number of PHX enzymes of the glycolysis pathway that well exceeds the number of PHX enzymes acting in the tricarboxylic acid cycle. Conversely, if the number of PHX enzymes of the tricarboxylic acid cycle well exceeds the PHX enzymes of glycolysis, an aerobic metabolism is preferred. Where the numbers are approximately commensurate, a facultative growth behavior prevails. Keywords: Archaea, Bacteria, predicted highly expressed, genomic comparisons, Drosophila The preceding paper ( 1) focused on the identity and analysis of predicted highly expressed (PHX) genes in archaeal genomes. In this context, a variety of chaperone proteins stand out, especially thermosome and prefoldin. This paper proffers a series of genomic and proteomic comparisons between Archaea and Bacteria plus corresponding results on PHX genes of the eukaryotes Saccharomyces cerevisiae and Drosophila melanogaster. Some Genomic Comparisons Between Archaea and Bacteria Ribosomal Protein (RP) Gene Organization. Many RP genes differ between most archaeal and bacterial genomes [see the clusters of orthologous groups of proteins (COG) database of the National Center for Biotechnology Information; see also ref. 2]. Most bacterial genomes possess a unique origin of replication and feature a large cluster (putative operon) nearby encompassing 15-40% of all RP genes. Generally, archaeal RP genes are confined to small clusters. Many genes involved in protein synthesis, including tuf, fus, rpoA, rpoB, rpoC, and some chaperones are encoded within or proximal to the large RP cluster in bacteria but not in archaea. In contrast, the RP genes of yeast (and of higher eukaryotes) are generally randomly dispersed throughout the genome. There are many introns in crenarchaeal protein-coding genes and tRNA genes but few or none among euryarchaeal genes. Extended 30-bp Repeats. All archaeal genomes, except Halobacterium sp., contain one or more clusters of 24-30 bp repeat elements, usually in excess of 50 copies, which are individually separated by 40-60 bp of unrelated sequences ( 3). Two types of 30-bp repeats occur for each of the crenarchaeal genomes and only one set for each euryarchaeal genome. A similar repeat arrangement is present in many thermophilic bacteria (table 4 of ref. 1). It is also observed in the genome of Bacillus halodurans, which is characterized as an extreme alkaliphilic bacterium living optimally in an environment of pH ≥9.5. The function of these repeats is unknown. Representations of Short Palindromes. Archaea and bacteria tend to show underrepresentations of 4- and 6-bp palindromes ( 4), but eukaryotes do not, consistent with avoidance of restriction systems in prokaryotic genomes. Unique Versus Multiple Origins of Replication. The GC skew [strand biases in (G - C)/(G + C) counts] ( 5- 7) shows a clear difference between archaea and bacteria, apparently related to the existence of unique vs. multiple origins of replication. Archaeal genomes often have multiple origins of replication. For example, three active oriC have been identified experimentally in Sulfolobus solfataricus (cf. refs. 8- 10). The Halobacterium genome carries at least two origins ( 11). It is argued that the Pyrococcus abyssi genome possesses a single origin ( 12, 13). The methanogens generally do not show any GC skew, and, on this basis, it is surmised that they possess multiple origins of replication. Some Proteomic Comparisons Between Archaea and Bacteria Protein and Amino Acids Synthesis and Replication Factors. The energy system of most archaea is autotrophic ( 14). Probably on this basis, several archaea synthesize the full collection of amino acids, including selenocysteine, and synthesize as well a wide assortment of cofactors, which is consistent with the tendency of Archaea to inhabit homogeneous extreme environments and concomitantly engage few PHX transport proteins. Translation elongation factors (e.g., EF-1α and EF-2) occur as single genes in archaeal genomes ( Table 1) but generally appear in multiple PHX copies in α-, β-, and γ-proteobacterial genomes. The ribosome release factor Rrf is found PHX in most bacteria and in yeast but is missing from archaea. The helicase protein RecG, which helps facilitate branch migration of the Holliday junction, is widespread in bacteria but not found in archaea ( 15). Presumably, archaea have other proteins to do these essential functions. | Table 1.Various comparisons of genomic and proteomic properties |
Membrane Lipid Biosynthesis. Organisms from all of the three domains of life contain polyisoprenes, but eukaryotes use significant amounts of sterols not abundant in either bacteria or archaea. Membranes of Gram-negative bacteria and eukaryotes are replete with phospholipids and lipid-modified proteins, whereas archaea generally emphasize prenylated ether lipids but make little or no fatty acids ( 16). Lipopolysaccharide biosynthesis genes of anomalous codon usage encode a hierarchy of surface antigens (the Lps family) that often occur in clusters. Lps biosynthesis genes are present in many bacterial and in most archaeal genomes but are not found in Gram-positive bacteria and apparently are not present in eukaryotes. The Gram-positive bacteria have lipoteichoic acid attached to their peptidoglycan, and these are weakly comparable to Lps of Gram-negative bacteria. The Lps complex also plays a role in cell adhesions. The lipid-A anchor (connecting the sugar and lipid moieties) prominent in Escherichia coli and Salmonella typhimurium appears to be missing from Gram-positive and archaeal genomes. The enzymatic apparatus for lipid synthesis is much reduced in most archaeal genomes. For example, FabB, FabD, and AcpP are not found in Archaea. According to the COG database, of 78 gene families involved in lipid metabolism extant in Bacteria, only 41 are also in Archaea, and none is unique to Archaea. Nitrogen Fixation ( nif) genes are present in several bacterial and archaeal genomes but not in eukaryotes. nif genes in archaea are evolutionarily related to nif genes in bacteria and operate by the same fundamental mechanism ( 17). It is proposed that some genes of this kind wander about by means of lateral gene transfer (e.g., as occurs in Klebsiella). The predominant nitrogenases in methanogens appear to be molybdenum nitrogenases as is the case in bacteria. The methanogens vary with respect to nitrogen fixation. For example, neither Methanococcus jannaschii nor Methanococcus volcanii fix nitrogen, whereas Methanosarcina barkeri and Methanococcus thermolithotropicus do ( 17). Glycolysis. Hexokinase and glucokinase are prominent glycolysis enzymes in eukaryotes, but the former is not found in most bacterial or in any archaeal genomes to date. Hexokinase converts glucose to glucose-6-phosphate. However, glucose-6-phosphate arises from other hexoses and from glucose transported into the cell by means of the phosphotransferase system (PTS). Bacteria that rely on carbohydrates as a primary energy source use the PTS system to transport glucose into the cytoplasm and concomitantly phosphorylate glucose making hexokinase/glucokinase expendable. PTS genes are apparently absent from all archaea. Generally, glycolysis genes in archaea are either not PHX or almost entirely missing. For example, glucose-phosphate isomerase is missing from the archaeon Archaeoglobus fulgidus and from Pyrococcus species, as well as from bacteria in the Mycoplasma group. Phosphofructokinase is missing from Archaea and several proteobacteria. There are no archaeal genomes with more than three (mostly one) glycolytic genes PHX. Tricarboxylic Acid (TCA) Cycle Genes. In aerobic environments, the TCA cycle, apart from production of energy, can contribute in myriad ways to cellular needs, especially in making precursors and intermediates to macromolecules, e.g., to amino acids, vitamins, and heme. All TCA cycle genes are present in archaeal genomes except in the methanogens and Pyrococcus species. RP Gene Numbers and PHX Accounts Comparing Archaeal and Bacterial Genomes The RP gene class, the TF (protein synthesis) gene ensemble and the major CH (chaperone/degradation) gene group are used as standards of codon usage biases for ascertaining PHX genes of bacterial genomes ( 1). In bacteria, usually (but not always) the RP genes comprise the most conspicuous PHX class of genes. However, RP genes of archaea do not comprise the most conspicuous PHX class of genes. Table 2 reports the count of RP genes of at least an 80-codon length across 34 diverse bacterial genomes, and Table 2 reports the count of RP genes of at least 80 codons in 19 archaeal genomes. (The requirement that a RP gene have a length of ≥80 codons allows the determination of the statistical validity or invalidity of the PHX property.) The number of these RP genes in archaeal genomes ( Table 2) range from 45 to 55 (average, 49.6; standard deviation, 2.65), whereas the range in bacterial genomes ( Table 2) is 39-46 (average, 43.4; standard deviation, 1.78). Actually, there are more RP genes in almost all archaeal genomes compared with almost all bacterial genomes. The contrast in numbers of RPs between archaeal and bacterial genomes is striking. The eukaryote (animals, fungi, and plants) ribosomal structure is composed of 79 or 80 RPs of all sizes. It is remarkable that 126 of 127 RP genes (these include many duplicates) in the yeast genome are PHX ( Table 2). All but a few of the RPs in each proteobacterial genome and in low G + C Gram-positive bacteria are PHX [manifest exceptions are the proteobacteria Helicobacter pylori and Campybacter jejuni ( Table 2)]. Apart from the methanogens ( Methanococcus maripaludis stands out, with all RPs of at least 80 aa PHX) in Archaea, generally only ≈60% of all RP genes ≥80 aa are PHX. Explicitly, among the bacterial genomes, an average of 37.5 RPs are PHX compared with an average of 30.4 PHX in archaeal genomes, indicating that many RP genes of archaea have reduced predicted expression levels akin to an average gene (see Table 2). The archaeal ribosome structure appears to be a small-scale model of the eukaryotic ribosome ( 2). | Table 2.Counts of PHX RP genes in archaeal, yeast, and bacterial genomes |
Lecompte et al. ( 2) proffer comparative analysis on the nature of RP summarizing distributions of 45 bacterial, 14 archaeal, and 7 eukaryotic genomes. Lecompte et al. ( 2) report a total of 78 RPs in Eukarya, 68 in Archaea, and 57 in Bacteria, and they postulate reductive evolution, i.e., the loss of RPs in the archaeal and bacterial lineages. Lecompte et al. ( 2) further observe that there are 34 RP genes shared by bacteria, archaea, and eukaryotes. There are also 33 RP genes shared by archaeal and eukaryotic genomes not found in any bacteria, zero RP genes common only to bacteria and archaea, and zero RP genes common to bacteria and eukaryotes consistent with the coevolution of archaea and eukaryotes. Eukaryotes are considered to have coevolved with an archaeal lineage, which might anticipate that the larger ribosome of eukaryotes relative to bacterial ribosomes implies an expanded ribosome structure in archaea versus bacteria. In summary, there are two primary anomalies in the numbers of RPs comprising the ribosome and in the PHX status of RPs in archaeal versus bacterial genomes. First, virtually all ribosomes of an archaeal genome are composed of more RPs than virtually all bacterial ribosomes (with very few exceptions; see Table 2). Secondly, the percent PHX of RPs among archaeal genomes is significantly less than that of bacterial genomes. What can account for these differences? ( i) The RNA of the ribosome in eukaryotes is larger and needs an expanded context to organize, stabilize, and facilitate the folding of the underlying rRNA. Also, an expanded ribosome cover may better protect the underlying RNA from ribonuclease cleavage. ( ii) Many eukaryote ribosome units interact with the ER membrane ( 18). This interaction may require an increased ribosomal complement and correspondingly more RP genes. ( iii) It is recognized in yeast that various chaperones, possibly including nascent polypeptide-associated complex, interact with ribosomes in processing and in protecting nascent polypeptides exiting the ribosome ( 19). ( iv) Archaea have representatives of bacterial and eukaryotic RPs, which may account for more RPs in archaeal as against bacterial genomes. ( v) Eukaryotic proteins are longer, on average (generally by at least 100 residues), than bacterial proteins ( 20- 22), which may require the size of the ribosomes to be larger. ( vi) Are the RP lengths generally longer in eukaryotes compared with bacteria? Actually, homologous RPs of eukaryotes tend to be longer than in bacteria ( 2). However, the longest RP overall is S1 in Gram-negative bacteria. ( vii) An alternative explanation might interpret the diminished numbers and sizes of RPs of the ribosome structure in bacteria as a consequence of streamlining the bacterial genome, which putatively increases efficiency. Are these comparisons of ribosome structural sizes and configurations correlated with slow growth for archaea? Examination of doubling times in Table 3 reveals that Pyrococcus, M. jannaschii, and M. maripaludis organisms are fast-growing, whereas the other archaea appear constrained to slow growth. In these terms, there appears to be no clear correlation between ribosome size and genome doubling time. A “giant” RP gene (designated S1) commonly exceeding 500 aa in length in Gram-negative bacteria is essential (with the exception of Mycoplasma). S1 is overall acidic and binds weakly and reversibly to the small subunit of the ribosome, whereas most other RPs bind strongly ( 23). S1 has a high affinity for mRNA chains, is necessary in many cases for translation initiation, is directly involved in mRNA recognition, and can facilitate binding of mRNA that lacks a strong Shine-Dalgarno motif. S1 is not encoded near any RP operon. The S1 proteins of low G + C Gram-positive bacteria (Firmicutes) are generally of reduced size [in the range of 360-410 aa ( 24)]. RPs are cationic (generally >20% cationic residues). The three acidic RPs found in eukaryotes, P 0, P 1, and P 2, are known to play an important regulatory role in the initiation step of eukaryotic mRNA translation. Of these, only P0 is present in archaea. The S2 RP gene in bacterial genomes is separated from other RPs, whereas S2 in many archaeal genomes is often incorporated in short RP clusters. In many bacterial genomes (e.g., Synechocystis and Mycobacterium tuberculosis), several major chaperone genes are proximal to the principal RP operon. For example, the major RP cluster in Synechocystis has GroEL-1 nearby. It is tempting to speculate that these chaperones contribute to ribosome formation. The deeply branching Gram-negative Aquifex aeolicus encodes a giant S1. Thermotoga maritima, allowing for a frameshift, also encodes an S1 homolog. All of the thermophilic bacteria displayed in table 4 of ref. 1 contain an S1. Unlike the giant bacterial S1, Saccharomyces cerevisiae RP genes are all <350 aa in length (generally between 50 and 350 aa) and are randomly dispersed over the 16 yeast chromosomes. Table 1 highlights various comparisons of genomic and proteomic characteristics within and between bacterial and archaeal genomes. For example, ( i) prokaryotic genomes often (but not always) employ Shine-Dalgarno motifs for translation initiation of mRNAs, whereas eukaryotes almost never use such controls. ( ii) Several bacterial genomes consist of multiple chromosomes, and several bacterial genomes feature linear chromosomes, but, to date, every archaeal genome has a single circular chromosome. Of course, because few archaeal genomes have been sequenced, the lack of multiple chromosomes may be sampling artifacts. ( iii) Chaperone proteins in archaea are like those in eukaryotes and feature prefoldin and thermosomes (TRi/CCT), with much fewer HSP70 gene representatives in archaea ( 1), whereas all bacterial genomes encode one or more HSP70 genes, usually PHX. To date, no human (or vertebrate) diseases have been associated with archaeal species ( 25- 27). Is this lack of pathogenic archaea due to the environment of human and archaea being fundamentally different? Martin ( 26) discusses the fundamental differences between vertebrate and archaeal biochemical workings and emphasizes the novel “cofactors” produced, especially in methanogens. The yeast genome somewhat parallels fast-growing bacteria in PHX genes augmented by actin, cofilin, profilin, tropomyosin and related genes. Most eukaryotic cells are spatially organized by the cytoskeleton containing three principal types of filaments: actin, microtubules, and intermediate filaments. Unlike mammalian cells, yeast cells do not contain intermediate filaments. Actin filaments occur in the cytoplasm and participate in various cellular activities, including cell budding, mating, defining cell polarity, transport, and maintenance of organelles ( 29). Actin is PHX at a very high expression level [ E( g) = 2.53]. Other PHX genes associated with actin [with E( g) values in parentheses] are cofilin (1.66), tropomyosin-1 (1.19), profilin (1.57), NADPH dehydrogenase (1.66), and myosin light chain (1.03). Cofilin controls reversibly actin polymerization and depolymerization in a pH-sensitive manner. Tropomyosin binds to and stabilizes actin filaments in the cell. Profilin plays a role in actin organization and maintenance of polarity. In contrast to actin filaments, microtubule and intermediate filament proteins are not PHX. NADPH is multifunctional, with its primary activity in energy metabolism. Microtubules are found in the cytoplasm and the nucleus, and they are cell cycle-regulated and play a major role in chromosome segregation and migration of the nucleus into the bud during mitosis. Microtubules are organized around a spindle pole body embedded in the nuclear envelope. Like microtubules, the spindle pole body components are not PHX. In contrast to mammalian cells, yeast contain very few microtubules, and they do not contribute significantly to cell shape or to transport of secretory vesicles as they do in mammalian cells. In yeast, microtubules are limited to a role in chromosomal segregation and nuclear migration. The difference in expression levels between actin filaments and microtubules is not surprising in view of the more specialized function of microtubules compared to actin filaments. Most prokaryotic genomes and especially fast-growing bacteria possess PHX DNA-directed RNA polymerase subunits, especially RpoB and RpoC. In contrast, none of the RNA polymerase II subunits in yeast is PHX. The same applies to RNA polymerases I and III. Dividing the transcription task among the three polymerases putatively reduces the need for high expression levels of each individual RNA polymerase. There may also be factors of growth rate and protein turnover. PHX genes in yeast appear randomly distributed among chromosomes in contrast to bacterial genomes, where PHX genes often form clusters of functionally related genes. Codon usage differences among different yeast chromosomes suggest that the smallest chromosome I is an outlier or a supernumerary chromosome. The other 15 chromosomes are substantially homogeneous in codon usages ( 30). In terms of codon usage differences and predicted expression levels, the genome of the unicellular yeast shows results similar to fast-growing bacteria. Among the top PHX genes are those encoding RPs, translation initiation, and elongation factors; a wide spectrum of chaperone proteins; enzymes functioning in glycolysis; and eukaryote-specific genes for actin, histones, and related genes. Histone genes are encoded in pairs as divergent neighbors {H3, H4} {H2A, H2B} on chromosome 2, another pair {H2B, H2A} on chromosome 4, and another pair {H3, H4} on chromosome 14. All histone genes except H1 are strongly PHX. Many metabolic genes are PHX, including almost all genes of glycolysis and gluconeogenesis and many fermentation genes; a series of genes of purine/pyrimidine synthesis, amino acid biogenesis, fatty acid synthesis, and sterol biosynthesis; a wide assortment of transporters (glucose transporters indicated earlier); phosphate transporters, including Pho84 and Pho88; uracil permease; and others. Altogether, 486 (8%) of 6,137 yeast genes with 80 or more codons score as PHX. Approximately 36% of all yeast genes are duplicated (i.e., have a paralog of significant sequence similarity). By contrast, 67% of PHX genes are duplicated, which may enhance the expression of these proteins. The yeast ribosome contains 78 RPs. Unlike bacterial genomes where RP genes are mostly organized in clusters and are not duplicated, the yeast RP gene ensemble consists mostly of duplicates distributed randomly throughout the genome. With a single exception, all cytoplasmic RP genes of at least an 80-codon length are PHX, generally with strikingly high predicted expression level, E( g) > 2.00. In contrast, the RPs functioning in the mitochondria generally encoded in the nucleus are never PHX and mostly score E( g) < 0.70, akin to an average gene. In yeast, there are at least 40 chaperone and degradation genes, and the majority are PHX. These genes include a family of HSP70 paralogs of distinct functions, as follows: SSB (two copies) are associated with ribosomes; SSA (two copies) act in trafficking polypeptides across mitochondrial membranes and into the endoplasmic reticulum; SSC assists in protein assembly and refolding in mitochondria; YDJ1 is involved in mitochondrial protein import; and PDR13 is associated with drug resistance. Other distinctive PHX chaperone proteins of yeast feature protein disulfide isomerase and HSP82. Ubiquitin contributes in ATP-dependent selective degradation of cellular proteins, the maintenance of chromatin structure, the stress response, ribosomal biogenesis, and DNA repair. There are many copies of E2 ubiquitin-conjugating enzymes that are PHX. Many seripauperin (stress induced) homologs are also PHX (e.g., PAU1-23). Yeast grows best on glucose, and it is not surprising that it contains an extended family of hexose transporters (HXT) with several members PHX at high levels. These PHX hexose transporters [with E( g) values in parentheses] are HXT1 (1.58), HXT2 (1.26), HXT3 (2.07), HXT4 (1.99), HXT6 (2.14), and HXT7 (2.16). Some other PHX transporters of yeast include phosphate transporters PHO84 (1.92), PHO88 (2.00), and MIR1 (mitochondrial; 1.53). BMH1 (1.14) and BMH2 (1.30) are PHX, which is surprising because they are regulatory proteins that participate in signal transduction pathways. However, they act stoichiometrically rather than catalytically, which may explain their PHX status. BMH1 and BMH2 are 14-3-3 proteins that are known to bind to phosphorylated proteins and regulate them by blocking critical protein-protein interactions ( 31). What gene classes are not PHX? As with bacteria, specialized regulatory proteins or proteins responding to special demands and required in few copies per cell cycle are not expected to be (and are not) PHX. For example, specialized transcription factors and cell cycle regulatory proteins are not PHX, similar to protein kinases and phosphatases. Genes acting in vitamin and cofactor biosynthesis pathways, of which only small amounts are needed to provide adequate function, have low predicted expression levels. Replication and repair enzymes are generally not PHX in bacteria or in yeast. PHX Genes of Drosophila melanogaster Among the transcripts that are ≥80 codons (including isoforms of the same gene), 2,338 (17%) genes are characterized as PHX. This percentage is higher than in bacteria and yeast, probably because of the more complex patterns, mixture of different specialized types of cells, and cellular requirements of higher eukaryotes. As in bacteria, the RPs, chaperones, translation/transcription processing factors, and major energy metabolism enzymes tend to be PHX. Conspicuously, structural skeletal proteins, such as spectrin, α-actinin, myosin, actin, and tubulin are found near the top of the list of PHX genes. Other eukaryote-specific genes among top PHX genes of Drosophila include larval serum proteins 1 and 2, alternative transcripts of a calcium transporter, and a chitinase. The following list highlights the top PHX genes. - Cytoskeletal and exoskeletal proteins [E(g) values mostly at ≥2.00], including spectrin, α-actinin, F-actin crosslinking protein, muscle myosin, actin, chitinase, tubulin, lumen, paramyosin, tropomyosin, troponin T, C, and chitin.
- Biosynthesis proteins [1.50 ≤ E(g) ≤ 2.00], including protein disulfide isomerase, Hsp90, Hsp70, Hsp60 (mitochondrial) (Tcp), proteasome subunits, thioredoxin-1, chaperone Cdc37, serine protease, and endopeptidase.
- Most RPs [1.50 ≤ E(g) ≤ 2.00], including P0, P1, and P2.
Aerobic Versus Anaerobic Preferences Table 4 reports the number of PHX enzymes in the two basic metabolic pathways, glycolysis and the TCA cycle, in >40 bacterial sequenced genomes, in 19 archaeal genomes, and in the S. cerevisiae and D. melanogaster eukaryotic genomes. The complete pathways carry 10 primary glycolytic genes and 15 primary TCA cycle genes. When the ratio of counts of PHX glycolysis genes to PHX TCA cycle genes is at least 2.5, we propose that the organism prefers an anaerobic metabolism, and where the ratio of PHX among TCA genes to glycolysis genes is at least 3, we declare a preference for an aerobic metabolism. We interpret the tendencies to be in favor of facultative growth when the ratios are rather commensurate. There are other situations for which the glycolytic and TCA cycle enzyme PHX sets are both low and for which we interpret the growth condition of the organism as primarily parasitic, symbiotic, or unknown. | Table 4.Counts of PHX genes of glycolysis and TCA cycle pathways in different genomes |
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