Abstract

Unicellular nitrogen-fixing cyanobacteria are important components of marine phytoplankton. Although non-nitrogen-fixing marine phytoplankton generally exhibit high gene sequence and genomic diversity, gene sequences of natural populations and isolated strains of Crocosphaera watsonii, one of the two most abundant open ocean unicellular cyanobacteria groups, have been shown to be 98–100% identical. The low sequence diversity in Crocosphaera is a dramatic contrast to sympatric species of Prochlorococcus and Synechococcus, and raises the question of how genome differences can explain observed phenotypic diversity among Crocosphaera strains. Here we show, through whole genome comparisons of two phenotypically different strains, that there are strain-specific sequences in each genome, and numerous genome rearrangements, despite exceptionally low sequence diversity in shared genomic regions. Some of the strain-specific sequences encode functions that explain observed phenotypic differences, such as exopolysaccharide biosynthesis. The pattern of strain-specific sequences distributed throughout the genomes, along with rearrangements in shared sequences is evidence of significant genetic mobility that may be attributed to the hundreds of transposase genes found in both strains. Furthermore, such genetic mobility appears to be the main mechanism of strain divergence in Crocosphaera which do not accumulate DNA microheterogeneity over the vast majority of their genomes. The strain-specific sequences found in this study provide tools for future physiological studies, as well as genetic markers to help determine the relative abundance of phenotypes in natural populations.

Highlights

  • Marine phytoplankton, which are dominated by cyanobacteria in most of the world’s open oceans, are important in global marine biogeochemical cycles and account for half of global carbon fixation (Waterbury et al, 1986; Goericke and Welschmeyer, 1993; Liu et al, 1997; Partensky et al, 1999; Scanlan and West, 2002)

  • There were an additional 227 contigs (0.4 Mb) that had no similarity to WH8501, but were identified as “probable” WH0003 genome sequence, based on similarity to other cyanobacterial sequences (Table 1)

  • The whole genome comparison of two Crocosphaera strains revealed that, the strains have divergent phenotypes, the vast majority of the two genomes are essentially identical at the nucleotide level, and only a small fraction of open reading frames (ORFs) in each genome are strain-specific

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Summary

Introduction

Marine phytoplankton, which are dominated by cyanobacteria in most of the world’s open oceans, are important in global marine biogeochemical cycles and account for half of global carbon fixation (Waterbury et al, 1986; Goericke and Welschmeyer, 1993; Liu et al, 1997; Partensky et al, 1999; Scanlan and West, 2002). More recent studies have reported high abundances using qPCR and direct cell counts (Zehr et al, 2001; Falcon et al, 2004; Church et al, 2005a, 2008; Langlois et al, 2008; Moisander et al, 2008, 2010), and measured high rates of in situ unicellular cyanobacterial N2 fixation (Zehr et al, 2001; Falcon et al, 2004; Montoya et al, 2004; Kitajima et al, 2009; Moisander et al, 2010), demonstrating that unicellular diazotrophs are often significant contributors of new N in the global ocean

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