Unveiling of Novel Radiations within Trichodesmium Cluster by hetR Gene Sequence Analysis

Department of Botany, Stockholm University, Stockholm, Sweden.
Applied and Environmental Microbiology (Impact Factor: 3.67). 02/2005; 71(1):190-6. DOI: 10.1128/AEM.71.1.190-196.2005
Source: PubMed


The filamentous nonheterocystous cyanobacterial genus Katagnymene is a common diazotrophic component of tropical and subtropical oceans. To assess the phylogenetic affiliation of this taxon,
two partial 16S rRNA gene sequences and 25 partial hetR gene sequences originating from the genera Katagnymene and Trichodesmium collected from open, surface waters of the Atlantic, Indian, and Pacific oceans were compared. Single trichomes or colonies
were identified morphologically by using light microscopy and then used directly as templates in hetR PCR analyses. In addition, three cultured strains, identified as Katagnymene pelagica, Katagnymene spiralis, and Trichodesmium sp., were examined. The data show that the genus Katagnymene is in the Trichodesmium cluster and that K. pelagica Lemmermann and K. spiralis Lemmermann are most likely one species, despite their different morphologies. Phylogenetic analyses also unveiled four distinct
clusters in the Trichodesmium cluster, including one novel cluster. Our findings emphasize the conclusion that known morphological traits used to differentiate
marine nonheterocystous cyanobacteria at the genus and species levels correlate poorly with genetic data, and a revision is
therefore suggested.

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    • "The high coverage of the HR-B and Trichodesmium metagenomes across their respective genomes shows that these populations were well represented in the sampled data. The relatively lower similarity between the Trichodesmium populations and the representative genome is similar to previous studies that investigated the diversity of Trichodesmium hetR gene fragments (Janson et al., 1999a; Lundgren et al., 2005; Hynes et al., 2012). In addition, if the gene content of the Trichodesmium populations varies from the T. erythraeum IMS101 reference genome just as the percent identity does, some of the Trichodesmium genes may be absent from the metagenome because they are not present in the genomes of the natural populations. "
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    ABSTRACT: Biological N2 fixation is an important nitrogen source for surface ocean microbial communities. However, nearly all information on the diversity and gene expression of organisms responsible for oceanic N2 fixation in the environment has come from targeted approaches that assay only a small number of genes and organisms. Using genomes of diazotrophic cyanobacteria to extract reads from extensive meta-genomic and -transcriptomic libraries, we examined diazotroph diversity and gene expression from the Amazon River plume, an area characterized by salinity and nutrient gradients. Diazotroph genome and transcript sequences were most abundant in the transitional waters compared with lower salinity or oceanic water masses. We were able to distinguish two genetically divergent phylotypes within the Hemiaulus-associated Richelia sequences, which were the most abundant diazotroph sequences in the data set. Photosystem (PS)-II transcripts in Richelia populations were much less abundant than those in Trichodesmium, and transcripts from several Richelia PS-II genes were absent, indicating a prominent role for cyclic electron transport in Richelia. In addition, there were several abundant regulatory transcripts, including one that targets a gene involved in PS-I cyclic electron transport in Richelia. High sequence coverage of the Richelia transcripts, as well as those from Trichodesmium populations, allowed us to identify expressed regions of the genomes that had been overlooked by genome annotations. High-coverage genomic and transcription analysis enabled the characterization of distinct phylotypes within diazotrophic populations, revealed a distinction in a core process between dominant populations and provided evidence for a prominent role for noncoding RNAs in microbial communities.The ISME Journal advance online publication, 16 December 2014; doi:10.1038/ismej.2014.240.
    Full-text · Article · Dec 2014 · The ISME Journal
    • "Despite decades of study, oceanic molecular surveys of Trichodesmium spp. frequently identify signatures from unidentified Trichodesmium phylotypes in field samples, demonstrating that not all members of this group have been recognized or characterized (Janson et al., 1999; Lundgren et al., 2005; Hynes et al., 2009; Chappell et al., 2012). Furthermore, relatively little is known about the distribution, specific microbial associations, enumeration and contribution of each of these phylotypes to Trichodesmium-specific global oceanic N 2 fixation (Hmelo et al., 2012). "
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    ABSTRACT: The cyanobacterial genus Trichodesmium is biogeochemically significant because of its dual role in nitrogen and carbon fixation in the oligotrophic ocean. Trichodesmium species form colonies that can be easily enriched from the water column and used for shipboard rate measurements to estimate their contribution to oceanic carbon and nitrogen budgets. During a July 2010 cruise near the Hawaiian Islands in the oligotrophic North Pacific Subtropical Gyre, a specific morphology of Trichodesmium puff-form colonies were examined under epifluorescent microscopy and found to harbor a colonial endobiont, morphologically identified as the heterocystous diazotrophic cyanobacterium Calothrix. Using unialgal enrichments obtained from this cruise, we show that these Calothrix-like heterocystous cyanobionts (hetDA for 'Trichodesmium-associated heterocystous diazotroph') fix nitrogen on a diurnal cycle (maximally in the middle of the light cycle with a detectable minimum in the dark). Gene sequencing of nifH from the enrichments revealed that this genus was likely not quantified using currently described quantitative PCR (qPCR) primers. Guided by the sequence from the isolate, new hetDA-specific primers were designed and subsequent qPCR of environmental samples detected this diazotroph from surface water to a depth of 150 m, reaching densities up to ∼9 × 10(3) l(-1). Based on phylogenetic relatedness of nifH and 16S rRNA gene sequences, it is predicted that the distribution of this cyanobiont is not limited to subtropical North Pacific but likely reaches to the South Pacific and Atlantic Oceans. Therefore, this previously unrecognized cohabitation, if it reaches beyond the oligotrophic North Pacific, could potentially influence Trichodesmium-derived nitrogen fixation budgets in the world ocean.
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    • "The non-heterocystous cyanobacterium Plectonema fixes nitrogen under microaerobic conditions only (Section III), while Lyngbya fixes nitrogen during the dark period of a light/dark cycle (Bergman et al., 1997). The non-heterocystous genus Trichodesmium uses a combination of a spatial (diazocytes) and temporal separation strategy with nitrogen fixation taking place in the light period as in heterocystous cyanobacteria (Berman-Frank et al., 2001; Lundgren et al., 2005). The various strategies are illustrated in Figure 2. "

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