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Molecular analysis of genes in Nostoc punctiforme involved in pilus biogenesis and plant infection.

ABSTRACT: Hormogonia are the infective agents in many cyanobacterium-plant symbioses. Pilus-like appendages are expressed on the hormogonium surface, and mutations in pil-like genes altered surface piliation and reduced symbiotic competency. This is the first molecular evidence that pilus biogenesis in a filamentous cyanobacterium requires a type IV pilus system.

SUBMITTER: Duggan PS

PROVIDER: S-EPMC1913353 | biostudies-literature | 2007 Jun

REPOSITORIES: biostudies-literature

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Molecular analysis of genes in Nostoc punctiforme involved in pilus biogenesis and plant infection.

Duggan Paula S PS Gottardello Priscila P Adams David G DG

Journal of bacteriology 20070406 12

Hormogonia are the infective agents in many cyanobacterium-plant symbioses. Pilus-like appendages are expressed on the hormogonium surface, and mutations in pil-like genes altered surface piliation and reduced symbiotic competency. This is the first molecular evidence that pilus biogenesis in a filamentous cyanobacterium requires a type IV pilus system. ...[more]

PMID: 17416648

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Project description:BackgroundThe last step in the maturation process of the large subunit of [NiFe]-hydrogenases is a proteolytic cleavage of the C-terminal by a hydrogenase specific protease. Contrary to other accessory proteins these hydrogenase proteases are believed to be specific whereby one type of hydrogenases specific protease only cleaves one type of hydrogenase. In cyanobacteria this is achieved by the gene product of either hupW or hoxW, specific for the uptake or the bidirectional hydrogenase respectively. The filamentous cyanobacteria Nostoc punctiforme ATCC 29133 and Nostoc sp strain PCC 7120 may contain a single uptake hydrogenase or both an uptake and a bidirectional hydrogenase respectively.ResultsIn order to examine these proteases in cyanobacteria, transcriptional analyses were performed of hupW in Nostoc punctiforme ATCC 29133 and hupW and hoxW in Nostoc sp. strain PCC 7120. These studies revealed numerous transcriptional start points together with putative binding sites for NtcA (hupW) and LexA (hoxW). In order to investigate the diversity and specificity among hydrogeanse specific proteases we constructed a phylogenetic tree which revealed several subgroups that showed a striking resemblance to the subgroups previously described for [NiFe]-hydrogenases. Additionally the proteases specificity was also addressed by amino acid sequence analysis and protein-protein docking experiments with 3D-models derived from bioinformatic studies. These studies revealed a so called "HOXBOX"; an amino acid sequence specific for protease of Hox-type which might be involved in docking with the large subunit of the hydrogenase.ConclusionOur findings suggest that the hydrogenase specific proteases are under similar regulatory control as the hydrogenases they cleave. The result from the phylogenetic study also indicates that the hydrogenase and the protease have co-evolved since ancient time and suggests that at least one major horizontal gene transfer has occurred. This co-evolution could be the result of a close interaction between the protease and the large subunit of the [NiFe]-hydrogenases, a theory supported by protein-protein docking experiments performed with 3D-models. Finally we present data that may explain the specificity seen among hydrogenase specific proteases, the so called "HOXBOX"; an amino acid sequence specific for proteases of Hox-type. This opens the door for more detailed studies of the specificity found among hydrogenase specific proteases and the structural properties behind it.

Project description:Scytonemin is a dimeric indole-phenol sunscreen synthesized by some cyanobacteria under conditions of exposure to UVA radiation. While its biosynthetic pathway has been elucidated only partially, comparative genomics reveals that the scytonemin operon often contains a cluster of five highly conserved genes (ebo cluster) of unknown function that is widespread and conserved among several bacterial and algal phyla. We sought to elucidate the function of the ebo cluster in the cyanobacterium Nostoc punctiforme by constructing and analyzing in-frame deletion mutants (one for each ebo gene and one for the entire cluster). Under conditions of UVA induction, all ebo mutants were scytoneminless, and all accumulated a single compound, the scytonemin monomer, clearly implicating all ebo genes in scytonemin production. We showed that the scytonemin monomer also accumulated in an induced deletion mutant of scyE, a non-ebo scytonemin gene whose product is demonstrably targeted to the periplasm. Confocal autofluorescence microscopy revealed that the accumulation was confined to the cytoplasm in all ebo mutants but that that was not the case in the scyE deletion, with an intact ebo cluster, where the scytonemin monomer was also excreted to the periplasm. The results implicate the ebo cluster in the export of the scytonemin monomer to the periplasm for final oxidative dimerization by ScyE. By extension, the ebo gene cluster may play similar roles in metabolite translocation across many bacterial phyla. We discuss potential mechanisms for such a role on the basis of structural and phylogenetic considerations of the ebo proteins.IMPORTANCE Elucidating the biochemical and genetic basis of scytonemin constitutes an interesting challenge because of its unique structure and the unusual fact that it is partially synthesized in the periplasmic space. Our work points to the ebo gene cluster, associated with the scytonemin operon of cyanobacteria, as being responsible for the excretion of scytonemin intermediates from the cytoplasm into the periplasm during biosynthesis. Few conserved systems have been described that facilitate the membrane translocation of small molecules. Because the ebo cluster is well conserved among a large diversity of bacteria and algae and yet insights into its potential function are lacking, our findings suggest that translocation of small molecules across the plasma membrane may be its generic role across microbes.

Dataset Information

Molecular analysis of genes in Nostoc punctiforme involved in pilus biogenesis and plant infection.

Publications

Molecular analysis of genes in Nostoc punctiforme involved in pilus biogenesis and plant infection.

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