Nitrogenase gene diversity and microbial community structure: a cross-system comparison

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Abstract

Biological nitrogen fixation is an important source of fixed nitrogen for the biosphere. Microorganisms catalyse biological nitrogen fixation with the enzyme nitrogenase, which has been highly conserved through evolution. Cloning and sequencing of one of the nitrogenase structural genes, nifH, has provided a large, rapidly expanding database of sequences from diverse terrestrial and aquatic environments. Comparison of nifH phylogenies to ribosomal RNA phylogenies from cultivated microorganisms shows little conclusive evidence of lateral gene transfer. Sequence diversity far outstrips representation by cultivated representatives. The phylogeny of nitrogenase includes branches that represent phylotypic groupings based on ribosomal RNA phylogeny, but also includes paralogous clades including the alternative, non-molybdenum, non-vanadium containing nitrogenases. Only a few alternative or archaeal nitrogenase sequences have as yet been obtained from the environment. Extensive analysis of the distribution of nifH phylotypes among habitats indicates that there are characteristic patterns of nitrogen fixing microorganisms in termite guts, sediment and soil environments, estuaries and salt marshes, and oligotrophic oceans. The distribution of nitrogen-fixing microorganisms, although not entirely dictated by the nitrogen availability in the environment, is non-random and can be predicted on the basis of habitat characteristics. The ability to assay for gene expression and investigate genome arrangements provides the promise of new tools for interrogating natural populations of diazotrophs. The broad analysis of nitrogenase genes provides a basis for developing molecular assays and bioinformatics approaches for the study of nitrogen fixation in the environment.

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Over three decades of molecular-phylogenetic studies, researchers have compiled an increasingly robust map of evolutionary diversification showing that the main diversity of life is microbial, distributed among three primary relatedness groups or domains: Archaea, Bacteria, and Eucarya. The general properties of representatives of the three domains indicate that the earliest life was based on inorganic nutrition and that photosynthesis and use of organic compounds for carbon and energy metabolism came comparatively later. The application of molecular-phylogenetic methods to study natural microbial ecosystems without the traditional requirement for cultivation has resulted in the discovery of many unexpected evolutionary lineages; members of some of these lineages are only distantly related to known organisms but are sufficiently abundant that they are likely to have impact on the chemistry of the biosphere.

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Cultivation of the ubiquitous SAR11 marine bacterioplankton clade.

Michael Rappé, Stephanie A. Connon, Kevin Vergin … (2002)

The alpha-proteobacterial lineage that contains SAR11 and related ribosomal RNA gene clones was among the first groups of organisms to be identified when cultivation-independent approaches based on rRNA gene cloning and sequencing were applied to survey microbial diversity in natural ecosystems. This group accounts for 26% of all ribosomal RNA genes that have been identified in sea water and has been found in nearly every pelagic marine bacterioplankton community studied by these methods. The SAR11 clade represents a pervasive problem in microbiology: despite its ubiquity, it has defied cultivation efforts. Genetic evidence suggests that diverse uncultivated microbial taxa dominate most natural ecosystems, which has prompted widespread efforts to elucidate the geochemical activities of these organisms without the benefit of cultures for study. Here we report the isolation of representatives of the SAR11 clade. Eighteen cultures were initially obtained by means of high-throughput procedures for isolating cell cultures through the dilution of natural microbial communities into very low nutrient media. Eleven of these cultures have been successfully passaged and cryopreserved for future study. The volume of these cells, about 0.01 micro m(3), places them among the smallest free-living cells in culture.

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J. Wu, W Sunda, E Boyle … (2000)

Surface waters of the subtropical Sargasso Sea contain dissolved inorganic phosphate (DIP) concentrations of 0.2 to 1.0 nanomolar, which are sufficiently low to result in phosphorus control of primary production. The DIP concentrations in this area (which receives high inputs of iron-rich dust from arid regions of North Africa) are one to two orders of magnitude lower than surface levels in the North Pacific (where eolian iron inputs are much lower and water column denitrification is much more substantial). These data indicate a severe relative phosphorus depletion in the Atlantic. We hypothesize that nitrogen versus phosphorus limitation of primary production in the present-day ocean may be closely linked to iron supply through control of dinitrogen (N2) fixation, an iron-intensive metabolic process. Although the oceanic phosphorus inventory may set the upper limit for the total amount of organic matter produced in the ocean over geological time scales, at any instant in geological time, oceanic primary production may fall below this limit because of a persistent insufficient iron supply. By controlling N2 fixation, iron may control not only nitrogen versus phosphorus limitation but also carbon fixation and export stoichiometry and hence biological sequestration of atmospheric carbon dioxide.