Open Access Research article

The mitochondrial and chloroplast genomes of the haptophyte Chrysochromulina tobin contain unique repeat structures and gene profiles

Blake T Hovde1, Shawn R Starkenburg2, Heather M Hunsperger3, Laina D Mercer4, Chloe R Deodato3, Ramesh K Jha2, Olga Chertkov2, Raymond J Monnat15 and Rose Ann Cattolico3*

Author Affiliations

1 Department of Genome Sciences, University of Washington, Seattle, WA, USA

2 Los Alamos National Laboratory, Bioscience Division, Los Alamos, NM, USA

3 Department of Biology, University of Washington, Seattle, WA, USA

4 Department of Statistics, University of Washington, Seattle, WA, USA

5 Department of Pathology, University of Washington, Seattle, WA, USA

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BMC Genomics 2014, 15:604  doi:10.1186/1471-2164-15-604

Published: 17 July 2014

Abstract

Background

Haptophytes are widely and abundantly distributed in both marine and freshwater ecosystems. Few genomic analyses of representatives within this taxon have been reported, despite their early evolutionary origins and their prominent role in global carbon fixation.

Results

The complete mitochondrial and chloroplast genome sequences of the haptophyte Chrysochromulina tobin (Prymnesiales) provide insight into the architecture and gene content of haptophyte organellar genomes. The mitochondrial genome (~34 kb) encodes 21 protein coding genes and contains a complex, 9 kb tandem repeat region. Similar to other haptophytes and rhodophytes, but not cryptophytes or stramenopiles, the mitochondrial genome has lost the nad7, nad9 and nad11 genes. The ~105 kb chloroplast genome encodes 112 protein coding genes, including ycf39 which has strong structural homology to NADP-binding nitrate transcriptional regulators; a divergent ‘CheY-like’ two-component response regulator (ycf55) and Tic/Toc (ycf60 and ycf80) membrane transporters. Notably, a zinc finger domain has been identified in the rpl36 ribosomal protein gene of all chloroplasts sequenced to date with the exception of haptophytes and cryptophytes - algae that have gained (via lateral gene transfer) an alternative rpl36 lacking the zinc finger motif. The two C. tobin chloroplast ribosomal RNA operon spacer regions differ in tRNA content. Additionally, each ribosomal operon contains multiple single nucleotide polymorphisms (SNPs) - a pattern observed in rhodophytes and cryptophytes, but few stramenopiles. Analysis of small (<200 bp) chloroplast encoded tandem and inverted repeats in C. tobin and 78 other algal chloroplast genomes show that repeat type, size and location are correlated with gene identity and taxonomic clade.

Conclusion

The Chrysochromulina tobin organellar genomes provide new insight into organellar function and evolution. These are the first organellar genomes to be determined for the prymnesiales, a taxon that is present in both oceanic and freshwater systems and represents major primary photosynthetic producers and contributors to global ecosystem stability.

Keywords:
Haptophytes; Chloroplast genome; Mitochondrial genome; Repeat structure; Repeat function; Chrysochromulina