In situ transcriptomic analysis of the globally important keystone N2-fixing taxon Crocosphaera watsonii
ABSTRACT The diazotrophic cyanobacterium Crocosphaera watsonii supplies fixed nitrogen (N) to N-depleted surface waters of the tropical oceans, but the factors that determine its distribution and contribution to global N(2) fixation are not well constrained for natural populations. Despite the heterogeneity of the marine environment, the genome of C. watsonii is highly conserved in nucleotide sequence in contrast to sympatric planktonic cyanobacteria. We applied a whole assemblage shotgun transcript sequencing approach to samples collected from a bloom of C. watsonii observed in the South Pacific to understand the genomic mechanisms that may lead to high population densities. We obtained 999 C. watsonii transcript reads from two metatranscriptomes prepared from mixed assemblage RNA collected in the day and at night. The C. watsonii population had unexpectedly high transcription of hypothetical protein genes (31% of protein-encoding genes) and transposases (12%). Furthermore, genes were expressed that are necessary for living in the oligotrophic ocean, including the nitrogenase cluster and the iron-stress-induced protein A (isiA) that functions to protect photosystem I from high-light-induced damage. C. watsonii transcripts retrieved from metatranscriptomes at other locations in the southwest Pacific Ocean, station ALOHA and the equatorial Atlantic Ocean were similar in composition to those recovered in the enriched population. Quantitative PCR and quantitative reverse transcriptase PCR were used to confirm the high expression of these genes within the bloom, but transcription patterns varied at shallower and deeper horizons. These data represent the first transcript study of a rare individual microorganism in situ and provide insight into the mechanisms of genome diversification and the ecophysiology of natural populations of keystone organisms that are important in global nitrogen cycling.
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ABSTRACT: Marine nitrogen-fixing cyanobacteria play a central role in the open-ocean microbial community by providing fixed nitrogen (N) to the ocean from atmospheric dinitrogen (N2) gas. Once thought to be dominated by one genus of cyanobacteria, Trichodesmium, it is now clear that marine N2-fixing cyanobacteria in the open ocean are more diverse, include several previously unknown symbionts, and are geographically more widespread than expected. The next challenge is to understand the ecological implications of this genetic and phenotypic diversity for global oceanic N cycling. One intriguing aspect of the cyanobacterial N2 fixers ecology is the range of cellular interactions they engage in, either with cells of their own species or with photosynthetic protists. From organelle-like integration with the host cell to a free-living existence, N2-fixing cyanobacteria represent the range of types of interactions that occur among microbes in the open ocean. Here, we review what is known about the cellular interactions carried out by marine N2-fixing cyanobacteria and where future work can help. Discoveries related to the functional roles of these specialized cells in food webs and the microbial community will improve how we interpret their distribution and abundance patterns and contributions to global N and carbon (C) cycles.Journal of Phycology 12/2013; 49(6). DOI:10.1111/jpy.12117 · 2.53 Impact Factor
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ABSTRACT: Crocosphaera watsonii, a unicellular nitrogen-fixing cyanobacterium found in oligotrophic oceans, is important in marine carbon and nitrogen cycles. Isolates of C. watsonii can be separated into at least two phenotypes with environmentally important differences, indicating possibly distinct ecological roles and niches. To better understand the evolutionary history and variation in metabolic capabilities among strains and phenotypes, this study compared the genomes of six C. watsonii strains, three from each phenotypic group, which had been isolated over several decades from multiple ocean basins. While a substantial portion of each genome was nearly identical to sequences in the other strains, a few regions were identified as specific to each strain and phenotype, some of which help explain observed phenotypic features. Overall, the small-cell type strains had smaller genomes and a relative loss of genetic capabilities, while the large-cell type strains were characterized by larger genomes, some genetic redundancy, and potentially increased adaptations to iron and phosphorus limitation. As such, strains with shared phenotypes were evolutionarily more closely related than those with the opposite phenotype, regardless of isolation location or date. Unexpectedly, the genome of the type-strain for the species, C. watsonii WH8501, was quite unusual even among strains with a shared phenotype, indicating it may not be an ideal representative of the species. The genome sequences and analyses reported in this study will be important for future investigations of the proposed differences in adaptation of the two phenotypes to nutrient limitation, and to identify phenotype-specific distributions in natural Crocosphaera populations.Journal of Phycology 08/2013; 49(4):786-801. DOI:10.1111/jpy.12090 · 2.53 Impact Factor
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ABSTRACT: Environmental (ecological) genomics aims to understand the genetic basis of relationships between organisms and their abiotic and biotic environments. It is a rapidly progressing field of research largely due to recent advances in the speed and volume of genomic data being produced by next generation sequencing (NGS) technologies. Building on information generated by NGS-based approaches, functional genomic methodologies are being applied to identify and characterize genes and gene systems of both environmental and evolutionary relevance. Marine photosynthetic organisms (MPOs) were poorly represented amongst the early genomic models, but this situation is changing rapidly. Here we provide an overview of the recent advances in the application of ecological genomic approaches to both prokaryotic and eukaryotic MPOs. We describe how these approaches are being used to explore the biology and ecology of marine cyanobacteria and algae, particularly with regard to their functions in a broad range of marine ecosystems. Specifically, we review the ecological and evolutionary insights gained from whole genome and transcriptome sequencing projects applied to MPOs and illustrate how their genomes are yielding information on the specific features of these organisms.Molecular Ecology 02/2013; 22(3):867-907. DOI:10.1111/mec.12000 · 5.84 Impact Factor