Molecular evolution of the nif gene cluster carrying nifI1 and nifI2 genes in the Gram-positive phototrophic bacterium Heliobacterium chlorum

Enkh-Amgalan, Jigjiddorj; Kawasaki, Hiroko; Seki, Tatsuji

doi:10.1099/ijs.0.63815-0

Cited by 18 publications

(16 citation statements)

References 46 publications

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“…4). The high level of similarity of heliobacterial nifHDK genes to the genes of Geobacter was also noted in phylogenetic analyses using nif genes from H. chlorum (15) (45). The products of nifI 1 and nifI 2 , which encode proteins belonging to the P II signal transduction family, are located between the nifH and nifD products in group II and III nitrogenases, but they are not present in most group I nitrogenases (15,45).…”

Section: Genome Properties H Modesticaldum Strain Ice1mentioning

confidence: 78%

“…H. modesticaldum is an active dinitrogen fixer, and this species and the green sulfur bacterium Chlorobaculum tepidum are the only cultured anoxygenic phototrophs that are capable of N 2 fixation at temperatures above 50°C (23,31). The organization of the nif regulon in H. modesticaldum is identical to that in Heliobacterium chlorum (15). The nif regulon consists of 11 genes: nifI 1 , nifI 2 , nifH, nifD, nifK, nifE, nifN, nifX, fdxB, nifB, and nifV.…”

Section: Genome Properties H Modesticaldum Strain Ice1mentioning

confidence: 91%

“…The products of nifI 1 and nifI 2 , which encode proteins belonging to the P II signal transduction family, are located between the nifH and nifD products in group II and III nitrogenases, but they are not present in most group I nitrogenases (15,45). The presence of nifI 1 and nifI 2 upstream of nifH in H. modesticaldum, as well as in other species of Heliobacterium and in D. hafniense Y51, suggests that the nitrogenase of these organisms may be an evolutionary intermediate between group I and group II/III nitrogenases (14,15).…”

Section: Genome Properties H Modesticaldum Strain Ice1mentioning

confidence: 99%

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The Genome of Heliobacterium modesticaldum , a Phototrophic Representative of the Firmicutes Containing the Simplest Photosynthetic Apparatus

et al. 2008

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Despite the fact that heliobacteria are the only phototrophic representatives of the bacterial phylum Firmicutes, genomic analyses of these organisms have yet to be reported. Here we describe the complete sequence and analysis of the genome of Heliobacterium modesticaldum, a thermophilic species belonging to this unique group of phototrophs. The genome is a single 3.1-Mb circular chromosome containing 3,138 open reading frames. As suspected from physiological studies of heliobacteria that have failed to show photoautotrophic growth, genes encoding enzymes for known autotrophic pathways in other phototrophic organisms, including ribulose bisphosphate carboxylase (Calvin cycle), citrate lyase (reverse citric acid cycle), and malyl coenzyme A lyase (3-hydroxypropionate pathway), are not present in the H. modesticaldum genome. Thus, heliobacteria appear to be the only known anaerobic anoxygenic phototrophs that are not capable of autotrophy. Although for some cellular activities, such as nitrogen fixation, there is a full complement of genes in H. modesticaldum, other processes, including carbon metabolism and endosporulation, are more genetically streamlined than they are in most other low-G؉C gram-positive bacteria. Moreover, several genes encoding photosynthetic functions in phototrophic purple bacteria are not present in the heliobacteria. In contrast to the nutritional flexibility of many anoxygenic phototrophs, the complete genome sequence of H. modesticaldum reveals an organism with a notable degree of metabolic specialization and genomic reduction.

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Section: Genome Properties H Modesticaldum Strain Ice1mentioning

confidence: 78%

Section: Genome Properties H Modesticaldum Strain Ice1mentioning

confidence: 91%

Section: Genome Properties H Modesticaldum Strain Ice1mentioning

confidence: 99%

See 1 more Smart Citation

The Genome of Heliobacterium modesticaldum , a Phototrophic Representative of the Firmicutes Containing the Simplest Photosynthetic Apparatus

et al. 2008

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“…In addition to these nitrogenase structural proteins, nif gene clusters can encode proteins involved in regulation (NifALI 1 I 2 ), electron transfer (NifFJ), and FeMo-co biosynthesis (NifXENBQUVYS), as well as proteins with as-yet-undefined functions (13). The functional composition of nif gene clusters varies considerably among taxa (5,8,14), where they range from the minimum gene complement known to encode an active nitrogenase (nifHDKEB) as well as several regulatory and uncharacterized genes (e.g., Methanocaldococcus sp. strain to those comprising Ͼ20 genes (e.g., Azotobacter vinelandii) (Fig.…”

Section: Importancementioning

confidence: 99%

Evolution of Molybdenum Nitrogenase during the Transition from Anaerobic to Aerobic Metabolism

Boyd¹,

Costas²,

Hamilton³

et al. 2015

J. Bacteriol.

117

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Molybdenum nitrogenase (Nif), which catalyzes the reduction of dinitrogen to ammonium, has modulated the availability of fixed nitrogen in the biosphere since early in Earth's history. Phylogenetic evidence indicates that oxygen (O 2 )-sensitive Nif emerged in an anaerobic archaeon and later diversified into an aerobic bacterium. Aerobic bacteria that fix N 2 have adapted a number of strategies to protect Nif from inactivation by O 2 , including spatial and temporal segregation of Nif from O 2 and respiratory consumption of O 2 . Here we report the complement of Nif-encoding genes in 189 diazotrophic genomes. We show that the evolution of Nif during the transition from anaerobic to aerobic metabolism was accompanied by both gene recruitment and loss, resulting in a substantial increase in the number of nif genes. While the observed increase in the number of nif genes and their phylogenetic distribution are strongly correlated with adaptation to utilize O 2 in metabolism, the increase is not correlated with any of the known O 2 protection mechanisms. Rather, gene recruitment appears to have been in response to selective pressure to optimize Nif synthesis to meet fixed N demands associated with aerobic productivity and to more efficiently regulate Nif under oxic conditions that favor protein turnover. Consistent with this hypothesis, the transition of Nif from anoxic to oxic environments is associated with a shift from posttranslational regulation in anaerobes to transcriptional regulation in obligate aerobes and facultative anaerobes. Given that fixed nitrogen typically limits ecosystem productivity, our observations further underscore the dynamic interplay between the evolution of Earth's oxygen, nitrogen, and carbon biogeochemical cycles. IMPORTANCEMolybdenum nitrogenase (Nif), which catalyzes the reduction of dinitrogen to ammonium, has modulated the availability of fixed nitrogen in the biosphere since early in Earth's history. Nif emerged in an anaerobe and later diversified into aerobes. Here we show that the transition of Nif from anaerobic to aerobic metabolism was accompanied by both gene recruitment and gene loss, resulting in a substantial increase in the number of nif genes. While the observed increase in the number of nif genes is strongly correlated with adaptation to utilize O 2 in metabolism, the increase is not correlated with any of the known O 2 protective mechanisms. Rather, gene recruitment was likely a response to more efficiently regulate Nif under oxic conditions that favor protein turnover.A ll life requires fixed nitrogen (N), and its availability often limits ecosystem productivity (1, 2). Most of the N on Earth is in the form of dinitrogen (N 2 ), which is unreactive, bio-unavailable, and must be chemically reduced to ammonium (NH 4 ϩ ) before it can be incorporated into biological molecules, such as proteins or nucleic acids. The primary enzyme that catalyzes the reduction of N 2 to NH 4 ϩ is the molybdenum (Mo)-dependent nitrogenase Nif (3, 4). Our recent phylogenetic studies...

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“…S1 in the supplemental material). According to the recent classification (11,30), the majority of OTUs (Ͼ80%) belong to the nifH group I gene, which corresponds to typical molybdenum-iron (Mo-Fe) nitrogenase. Cyanobacteria were absent from wild stands, and there were more clones related to Deltaproteobacteria cluster B in the Wild-VC stand.…”

Section: Dotur Analysismentioning

confidence: 99%

No Evidence of an Impact on the Rhizosphere Diazotroph Community by the Expression of Bacillus thuringiensis Cry1Ab Toxin by Bt White Spruce

Lamarche

Hamelin

2007

Appl Environ Microbiol

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Nitrogen fixation is one of the most important roles played by soil bacterial communities, as fixation supplies nitrogen to many ecosystems which are often N limited. As impacts on this functional group of bacteria might harm the ecosystem's health and reduce productivity, monitoring that particular group is important. Recently, a field trial with Bt white spruce, which constitutively expresses the Cry1Ab insecticidal toxin of Bacillus thuringiensis, was established. The Bt white spruce was shown to be resistant to spruce budworm. We investigated the possible impact of these genetically modified trees on soil nitrogen-fixing bacterial communities. The trial consisted of untransformed controls, GUS white spruce (transformed with the ␤-glucuronidase gene), and Bt/GUS white spruce (which constitutively expresses both the Cry1Ab toxin and ␤-glucuronidase) in a random design. Four years after planting, soil samples from the control and the two treatments from plantation as well as from two natural stands of white spruce were collected. Diazotroph diversity was assessed by extracting soil genomic DNA and amplifying a region of the nitrogenase reductase (nifH) gene, followed by cloning and sequencing. Analysis revealed that nitrogen-fixing communities did not differ significantly among the untransformed control, GUS white spruce, and Bt/GUS white spruce. Nevertheless, differences in diazotroph diversity were observed between white spruce trees from the plantation site and those from two natural stands, one of which grew only a few meters away from the plantation. We therefore conclude, in the absence of evidence that the presence of the B. thuringiensis cry1Ab gene had an effect on diazotroph communities, that either site and/or field preparation prior to planting seems to be more important in determining diazotroph community structure than the presence of Bt white spruce.

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Molecular evolution of the nif gene cluster carrying nifI1 and nifI2 genes in the Gram-positive phototrophic bacterium Heliobacterium chlorum

Cited by 18 publications

References 46 publications

The Genome of Heliobacterium modesticaldum , a Phototrophic Representative of the Firmicutes Containing the Simplest Photosynthetic Apparatus

The Genome of Heliobacterium modesticaldum , a Phototrophic Representative of the Firmicutes Containing the Simplest Photosynthetic Apparatus

Evolution of Molybdenum Nitrogenase during the Transition from Anaerobic to Aerobic Metabolism

No Evidence of an Impact on the Rhizosphere Diazotroph Community by the Expression of Bacillus thuringiensis Cry1Ab Toxin by Bt White Spruce

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