Genetic regulation of nitrogen fixation in rhizobia.

Cyanobacteria may possess several enzymes that are directly involved in dihydrogen metabolism: nitrogenase(s) catalyzing the production of hydrogen concomitantly with the reduction of dinitrogen to ammonia, an uptake hydrogenase (encoded by hupSL) catalyzing the consumption of hydrogen produced by the nitrogenase, and a bidirectional hydrogenase (encoded by hoxFUYH) which has the capacity to both take up and produce hydrogen. This review summarizes our knowledge about cyanobacterial hydrogenases, focusing on recent progress since the first molecular information was published in 1995. It presents the molecular knowledge about cyanobacterial hupSL and hoxFUYH, their corresponding gene products, and their accessory genes before finishing with an applied aspect—the use of cyanobacteria in a biological, renewable production of the future energy carrier molecular hydrogen. In addition to scientific publications, information from three cyanobacterial genomes, the unicellular Synechocystis strain PCC 6803 and the filamentous heterocystous Anabaena strain PCC 7120 and Nostoc punctiforme (PCC 73102/ATCC 29133) is included.

https://mmbr.asm.org/content/mmbr/66/1/1.full.pdf

Hydrogenases and Hydrogen Metabolism of Cyanobacteria

Nickel is one of 23 metal pollutants of great concern to the environment and to human health (Sunderman 1992; Jarup 2003; Duda-Chodak and Baszczyk 2008). Nickel is the 24th most abundant element (twice as Cu) and comprises approximately 0.008% of the content of the earth’s crust; hence, it is a natural component of soil (parent material) and water (Alloway 1995; Hostýnek and Maibach 2002; Hedfi et al. 2007). Most of the earth’s nickel, however, is inaccessible, as it is locked in the iron–nickel molten core, which constitutes approximately 10% nickel. The second largest Ni deposits of the earth rest in the sea. It is estimated that the sea contains approximately eight billion tons of Ni, either dissolved in seawater or deposited in the seabed (Birch 1964; Stixrude et al. 1997). Soils may contain nickel levels as low as 0.2 mg kg−1 or as high as 450 mg kg−1. The average nickel content in soil is approximately 20 mg kg−1; however, the content level may vary greatly depending upon the mode of origin of the soil’s parent material (Assembly of Life Sciences 1975; Aubert and Pinta 1978; Wilson and Kordybach 2000). Because organic matter strongly absorbs some metals, particularly nickel, fossil fuels such as coal and oil may contain considerable amounts of nickel (Sigel et al. 2005). Moreover, Ni naturally occurs in a few plants (legumes) where it functions as an essential component of some enzymes (e.g., ureases) that are involved in nitrogen assimilation (Eskew et al. 1984; Brown et al. 1987a; Sakamoto and Bryant 2001).

Essential Roles and Hazardous Effects of Nickel in Plants

Oxidation of molecular hydrogen catalyzed by [NiFe] hydrogenases is a widespread mechanism of energy generation among prokaryotes. Biosynthesis of the H2-oxidizing enzymes is a complex process subject to positive control by H2 and negative control by organic energy sources. In this report we describe a novel signal transduction system regulating hydrogenase gene (hox) expression in the proteobacterium Alcaligenes eutrophus. This multicomponent system consists of the proteins HoxB, HoxC, HoxJ*, and HoxA. HoxB and HoxC share characteristic features of dimeric [NiFe] hydrogenases and form the putative H2 receptor that interacts directly or indirectly with the histidine protein kinase HoxJ*. A single amino acid substitution (HoxJ*G422S) in a conserved C-terminal glycine-rich motif of HoxJ* resulted in a loss of H2-dependent signal transduction and a concomitant block in autophosphorylating activity, suggesting that autokinase activity is essential for the response to H2. Whereas deletions in hoxB or hoxC abolished hydrogenase synthesis almost completely, the autokinase-deficient strain maintained high-level hox gene expression, indicating that the active sensor kinase exerts a negative effect on hox gene expression in the absence of H2. Substitutions of the conserved phosphoryl acceptor residue Asp55 in the response regulator HoxA (HoxAD55E and HoxAD55N) disrupted the H2 signal-transduction chain. Unlike other NtrC-like regulators, the altered HoxA proteins still allowed high-level transcriptional activation. The data presented here suggest a model in which the nonphosphorylated form of HoxA stimulates transcription in concert with a yet unknown global energy-responsive factor.

https://www.pnas.org/content/pnas/95/21/12474.full.pdf

A novel multicomponent regulatory system mediates H2 sensing in Alcaligenes eutrophus.

Nucleotide sequence analysis revealed a 1,791-bp open reading frame in the hox gene cluster of the gram-negative chemolithotroph Alcaligenes eutrophus H16. In order to investigate the biological role of this open reading frame, we generated an in-frame deletion allele via a gene replacement strategy. The resulting mutant grew significantly more slowly than the wild type under lithoautotrophic conditions (6.1 versus 4.2 h doubling time). A reduction in the level of the soluble NAD-reducing hydrogenase (60% of the wild-type activity) was shown to be the cause of the slow lithoautotrophic growth. We used plasmid-borne gene fusions to monitor the expression of the operons encoding the soluble and membrane-bound hydrogenases. The expression of both operons was lower in the mutant than in the wild-type strain. These results suggest that the newly identified gene, designated hoxX, encodes a regulatory component which, in conjunction with the transcriptional activator HoxA, controls hydrogenase synthesis.

The Alcaligenes eutrophus H16 hoxX gene participates in hydrogenase regulation.

In Bradyrhizobium japonicum, Tn5 insertions in a particular chromosomal DNA fragment result in a Hup− phenotype in free-living conditions without affecting hydrogenase (Hup) activity in the symbiotic state. By determination of the nucleotide sequence of this region, we were able to identify the nature of the inactivated genes. The fragment is located 9 kb downstream of the hydrogenase structural genes and contains one incomplete and three complete open reading frames. They are designated hypD′, hypE, hoxX and hoxA respectively, since the deduced amino acid sequences display very strong homology with genes involved in the regulation of hydrogenase activity in Escherichia coli, Rhodobacter capsulatus, Azotobacter vinelandii (hypD′ and hypE) and Alcaligenes eutrophus (hoxX and hoxA). This is the first report on transcriptional activators of the hup genes in B. japonicum. Implications of these findings with respect to regulation of hydrogenase synthesis by hydrogen, oxygen and nickel in free-living B. japonicum are discussed.

Identification of a potential transcriptional regulator of hydrogenase activity in free-living Bradyrhizobium japonicum strains.

Nucleotide Sequence Analysis of Four Genes, hupC, hupD, hupF and hupG, Downstream of the Hydrogenase Structural Genes in Bradyrhizobium japonicum

A region of 15 kbp DNA located on the chromosome of Bradyrhizobium japonicum is essential for a Hup(+) phenotype and contains the hydrogenase structural genes. During the last few years, other genes with various functions related to hydrogenase oxidation, such as Ni(2+) incorporation into the hydrogenase enzyme, electron transport from hydrogenase to O2, and regulation of hydrogenase expression in free-living conditions, have been identified in this region. A region in front of the hydrogenase structural genes is necessary for transcriptional regulation of hydrogenase expression by O2, H2 and Ni(2+). In addition, the N2 fixation system and the tertiary structure of the chromosome seem to be involved in the expression of the hydrogenase genes. The effect of legume inoculation with Hup(+) rhizobia has been evaluated. The possible benefits of a Hup(+) phenotype, such as the regeneration of chemical energy in the form of ATP or reductants, and the removal of O2 and H2 from the active site of the nitrogenase enzyme where they might inhibit the nitrogenase reaction, are discussed. The data indicate that a H2-uptake system is beneficial in soybean nodules, but host plant and environmental factors may interfere with the effects of H2 cycling in the plant.

Hydrogenase in Bradyrhizobium japonicum: genetics, regulation and effect on plant growth.

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Identification of a potential transcriptional regulator of hydrogenase activity in free-living Bradyrhizobium japonicum strains.

Nucleotide Sequence Analysis of Four Genes, hupC, hupD, hupF and hupG, Downstream of the Hydrogenase Structural Genes in Bradyrhizobium japonicum

Hydrogenase in Bradyrhizobium japonicum: genetics, regulation and effect on plant growth.