The Stigmatella aurantiaca homolog of Myxococcus xanthus high-mobility-group A-type transcription factor CarD: insights into the functional modules of CarD and their distribution in bacteria.
Transcriptional factor CarD is the only reported prokaryotic analog of eukaryotic high-mobility-group A (HMGA) proteins, in that it has contiguous acidic and AT hook DNA-binding segments and multifunctional roles in Myxococcus xanthus carotenogenesis and fruiting body formation. HMGA proteins are small, randomly structured, nonhistone, nuclear architectural factors that remodel DNA and chromatin structure. Here we report on a second AT hook protein, CarD(Sa), that is very similar to CarD and that occurs in the bacterium Stigmatella aurantiaca. CarD(Sa) has a C-terminal HMGA-like domain with three AT hooks and a highly acidic adjacent region with one predicted casein kinase II (CKII) phosphorylation site, compared to the four AT hooks and five CKII sites in CarD. Both proteins have a nearly identical 180-residue N-terminal segment that is absent in HMGA proteins. In vitro, CarD(Sa) exhibits the specific minor-groove binding to appropriately spaced AT-rich DNA that is characteristic of CarD or HMGA proteins, and it is also phosphorylated by CKII. In vivo, CarD(Sa) or a variant without the single CKII phosphorylation site can replace CarD in M. xanthus carotenogenesis and fruiting body formation. These two cellular processes absolutely require that the highly conserved N-terminal domain be present. Thus, three AT hooks are sufficient, the N-terminal domain is essential, and phosphorylation in the acidic region by a CKII-type kinase can be dispensed with for CarD function in M. xanthus carotenogenesis and fruiting body development. Whereas a number of hypothetical proteins homologous to the N-terminal region occur in a diverse array of bacterial species, eukaryotic HMGA-type domains appear to be confined primarily to myxobacteria.
Cayuela
María L
ML
Departamento de Genética y Microbiología, Universidad de Murcia, 30100 Murcia, Spain.
Elías-Arnanz
Montserrat
M
Peñalver-Mellado
Marcos
M
Padmanabhan
S
S
Murillo
Francisco J
FJ
D024761:AT-Hook Motifs / Q000235:genetics; D000595:Amino Acid Sequence; D001426:Bacterial Proteins; D015139:Blotting, Southern; D047390:Casein Kinase II; D004268:DNA-Binding Proteins / Q000235:genetics / Q000378:metabolism; D017353:Gene Deletion; D005816:Genetic Complementation Test; D008969:Molecular Sequence Data; D016941:Myxococcus xanthus / Q000235:genetics; D010766:Phosphorylation; D017346:Protein Serine-Threonine Kinases / Q000378:metabolism; D016415:Sequence Alignment; D013045:Species Specificity; D020606:Stigmatella aurantiaca / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D015534:Trans-Activators / Q000096:biosynthesis / Q000235:genetics / Q000378:metabolism*
D001426:Bacterial Proteins; C100589:CarD protein, Myxococcus xanthus; D004268:DNA-Binding Proteins; D015534:Trans-Activators; D047390:Casein Kinase II; D017346:Protein Serine-Threonine Kinases