Horizontal transfer of the nitrogen fixation gene cluster in the cyanobacterium <i>Microcoleus chthonoplastes</i>

Bolhuis, Henk; Severin, Ina; Confurius-Guns, Veronique; Wollenzien, Ute; Stal, Lucas J.

doi:10.1038/ismej.2009.99

Cited by 109 publications

(85 citation statements)

References 38 publications

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“…The genes with the highest K values were nifI 1 /nifI 2 (K ϭ 4.18; P ϭ 0.001), nifW (K ϭ 1.36; P ϭ 0.001), and nifZ (K ϭ 1.26; P ϭ 0.001). These observations suggest a general trend of recruitment and vertical inheritance of nif genes, although gene loss (e.g., nifI 1 and nifI 2 ) and horizontal gene transfer events have also impacted the evolution of Nif (3,7,8,44).…”

Section: Resultsmentioning

confidence: 98%

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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Section: Resultsmentioning

confidence: 98%

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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“…Microcoleus chthonoplastes, the type strain for mat-dwelling Microcoleus spp., was for many years not thought to be a diazotrophic cyanobacterium. However, the recently completed genome of M. chthonoplastes PCC 7420 revealed a nif-gene cluster (Bolhuis et al, 2010) …”

Section: Discussionmentioning

confidence: 99%

Identification of a novel cyanobacterial group as active diazotrophs in a coastal microbial mat using NanoSIMS analysis

et al. 2012

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N2 fixation is a key process in photosynthetic microbial mats to support the nitrogen demands associated with primary production. Despite its importance, groups that actively fix N2 and contribute to the input of organic N in these ecosystems still remain largely unclear. To investigate the active diazotrophic community in microbial mats from the Elkhorn Slough estuary, Monterey Bay, CA, USA, we conducted an extensive combined approach, including biogeochemical, molecular and high-resolution secondary ion mass spectrometry (NanoSIMS) analyses. Detailed analysis of dinitrogenase reductase (nifH) transcript clone libraries from mat samples that fixed N2 at night indicated that cyanobacterial nifH transcripts were abundant and formed a novel monophyletic lineage. Independent NanoSIMS analysis of 15N2-incubated samples revealed significant incorporation of 15N into small, non-heterocystous cyanobacterial filaments. Mat-derived enrichment cultures yielded a unicyanobacterial culture with similar filaments (named Elkhorn Slough Filamentous Cyanobacterium-1 (ESFC-1)) that contained nifH gene sequences grouping with the novel cyanobacterial lineage identified in the transcript clone libraries, displaying up to 100% amino-acid sequence identity. The 16S rRNA gene sequence recovered from this enrichment allowed for the identification of related sequences from Elkhorn Slough mats and revealed great sequence diversity in this cluster. Furthermore, by combining 15N2 tracer experiments, fluorescence in situ hybridization and NanoSIMS, in situ N2 fixation activity by the novel ESFC-1 group was demonstrated, suggesting that this group may be the most active cyanobacterial diazotroph in the Elkhorn Slough mat. Pyrotag sequences affiliated with ESFC-1 were recovered from mat samples throughout 2009, demonstrating the prevalence of this group. This work illustrates that combining standard and single-cell analyses can link phylogeny and function to identify previously unknown key functional groups in complex ecosystems.

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“…NifH genes are present in a broad spectrum of prokaryotes, and the phylogenetic relationships among these organisms based on nifH sequences are largely congruent with those determined from 16S rRNA gene sequences (Zehr et al 2003b). This suggests that horizontal gene transfer of the nifH gene has been limited (Zehr et al 2003b), although it has been observed for several bacterial species (Raymond et al 2004, Kechris et al 2006, Bolhuis et al 2010. Consequently, nifH sequences are used to tentatively infer phylogenetic affiliations of diazotrophs in microbial communities.…”

Section: Nitrogenase Genes From Non-cyanobacteria Are Widespread In Mmentioning

confidence: 99%

Nitrogenase genes in non-cyanobacterial plankton: prevalence, diversity and regulation in marine waters

Riemann

Farnelid²,

Steward³

2010

Aquat. Microb. Ecol.

164

165

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Marine waters are generally considered to be nitrogen (N) limited and are therefore favourable environments for diazotrophs, i.e. organisms converting atmospheric N 2 into ammonium or nitrogen oxides available for growth. In some regions, this import of N supports up to half of the primary productivity. Diazotrophic Cyanobacteria appear to be the major contributors to marine N 2 fixation in surface waters, whereas the contribution of heterotrophic or chemoautotrophic diazotrophs to this process is usually regarded inconsequential. Culture-independent studies reveal that non-cyanobacterial diazotrophs are diverse, widely distributed, and actively expressing the nitrogenase gene in marine and estuarine environments. The detection of nifH genes and nifH transcripts, even in N-replete marine waters, suggests that N 2 fixation is an ecologically important process throughout the oceans. Because this process is highly sensitive to and inhibited by molecular oxygen (O 2 ), diazotrophy requires efficient scavenging of intracellular O 2 or growth in environments with low ambient O 2 concentration. Particles with interior low-O 2 micro-zones and oceanic oxygen minimum zones are just 2 potential habitats suitable for N 2 fixation by non-cyanobacterial diazotrophs. Our ignorance about the regulation of N 2 fixation by non-Cyanobacteria in their natural marine environments currently prevents an evaluation of their importance in marine N cycling and budgets. A review of the molecular data on distribution and expression of nifH genes in non-Cyanobacteria suggests that further study of the role of these Bacteria in N cycling at local, regional and global scales is needed.KEY WORDS: N 2 fixation · Nitrogen fixation · Non-Cyanobacteria · nifH · Nitrogenase Resale or republication not permitted without written consent of the publisher Contribution to AME Special 4 'Progress and perspectives in aquatic microbial ecology'OPEN PEN ACCESS CCESS

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Horizontal transfer of the nitrogen fixation gene cluster in the cyanobacterium Microcoleus chthonoplastes

Cited by 109 publications

References 38 publications

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

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

Identification of a novel cyanobacterial group as active diazotrophs in a coastal microbial mat using NanoSIMS analysis

Nitrogenase genes in non-cyanobacterial plankton: prevalence, diversity and regulation in marine waters

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