Low genomic diversity in tropical oceanic N ₂ -fixing cyanobacteria

Abstract

High levels of genomic and allelic microvariation have been found in major marine planktonic microbial species, including the ubiquitous open ocean cyanobacterium, Prochlorococcus marinus. Crocosphaera watsonii is a unicellular cyanobacterium that has recently been shown to be important in oceanic N2 fixation and has been reported from the Atlantic and Pacific oceans in both hemispheres, and the Arabian Sea. In direct contrast to the current observations of genomic variability in marine non-N2-fixing planktonic cyanobacteria, which can range up to >15% nucleotide sequence divergence, we discovered that the marine planktonic nitrogen-fixing cyanobacterial genus Crocosphaera has remarkably low genomic diversity, with <1% nucleotide sequence divergence in several genes among widely distributed populations and strains. The cultivated C. watsonii WH8501 genome sequence was virtually identical to DNA sequences of large metagenomic fragments cloned from the subtropical North Pacific Ocean with <1% sequence divergence even in intergenic regions. Thus, there appears to be multiple strategies for evolution, adaptation, and diversification in oceanic microbial populations. The C. watsonii genome contains multiple copies of several families of transposases that may be involved in maintaining genetic diversity through genome rearrangements. Although genomic diversity seems to be the rule in many, if not most, marine microbial lineages, different forces may control the evolution and diversification in low abundance microorganisms, such as the nitrogen-fixing cyanobacteria.evolution ͉ genome ͉ marine ͉ nitrogen fixation ͉ Crocosphaera

In situ transcriptomic analysis of the globally important keystone N2-fixing taxon Crocosphaera watsonii

“…This corresponded with a greater number of C. watsonii WH8501 recombination and repair orthologs (7.1-10.7% of all transcripts) than in the dominant sympatric cyanobacterium, Prochlorococcus marinus MIT9301 (2.0-2.7% of all transcripts), which lacks transposase genes altogether. Our results are consistent with a metatranscriptome sequencing effort from station ALOHA in the North Pacific Ocean, where 3 transposase sequences were recovered from 50 total C. watsonii WH8501 transcripts (Zehr et al, 2007a). Transposases were also recovered at other locations in the southwest Pacific Ocean and equatorial North Atlantic Ocean, but represented a smaller percentage of total C. watsonii WH8501 transcripts (Supplementary Table 1).…”

“…It has been hypothesized that genetic diversity in C. watsonii may be maintained by genome rearrangement, rather than by gene sequence divergence because the diazotroph has low levels of genome DNA sequence variability between habitats and over time (Zehr et al, 2007a). High transposase activity in C. watsonii is similar to that found in populations of the archaeon Ferroplasma acidarmanus (Allen et al, 2007), and positive selection of transposases has been linked to increased fitness or invasion of new environments (Mes and Doeleman, 2006;Allen et al, 2007;Franguel et al, 2008).…”

“…High transposase activity in C. watsonii is similar to that found in populations of the archaeon Ferroplasma acidarmanus (Allen et al, 2007), and positive selection of transposases has been linked to increased fitness or invasion of new environments (Mes and Doeleman, 2006;Allen et al, 2007;Franguel et al, 2008). The C. watsonii WH8501 genome has a large number of transposases (419 transposases in the B6.3 Mb genome), some of which interrupt reading frames of genes (Zehr et al, 2007a) and may result in phenotypic diversity. The activity of transposases may be linked to gene modification or silencing.…”

“…In most metagenomic sequencing efforts (Venter et al, 2004), microdiversity of dominant prokaryotic groups (Brown and Fuhrman, 2005;Garcia-Martinez and RodriguezValera, 2000) complicates assembly and taxonomic identification of short genomic fragments. C. watsonii has an unusually high degree of genome conservation, with similar nucleotide composition between strains isolated two decades ago and bacterial artificial chromosome-cloned genomic fragments obtained from station ALOHA in 2005 (Zehr et al, 2007a). Because C. watsonii has a high degree of genome conservation, metagenomic and metatranscriptomic studies are relatively simple as sequence reads identical to the C. watsonii WH8501 genome can be isolated even among complex read libraries.…”

Distribution of microbial terpenoid lipid cyclases in the global ocean metagenome

“…In contrast, although the absence of cyanobacterial SHC sequences in the GOS samples does not mean that cyanobacterial producers of hopanoids are absent from the presentday ocean (they surely are present, for example, Crocosphaera watsonii and Trichodesmium erythraeum; Capone et al, 1997;Zehr et al, 2001Zehr et al, , 2007, their proportional density among total hopanoid producers appears to be low.…”