The chloroplast genomes of Bryopsis plumosa and Tydemania expeditiones (Bryopsidales, Chlorophyta): compact genomes and genes of bacterial origin.

Frederik Leliaert,Juan M Lopez-Bautista

doi:10.1186/s12864-015-1418-3

Abstract

BackgroundSpecies of Bryopsidales form ecologically important components of seaweed communities worldwide. These siphonous macroalgae are composed of a single giant tubular cell containing millions of nuclei and chloroplasts, and harbor diverse bacterial communities. Little is known about the diversity of chloroplast genomes (cpDNAs) in this group, and about the possible consequences of intracellular bacteria on genome composition of the host. We present the complete cpDNAs of Bryopsis plumosa and Tydemania expeditiones, as well as a re-annotated cpDNA of B. hypnoides, which was shown to contain a higher number of genes than originally published. Chloroplast genomic data were also used to evaluate phylogenetic hypotheses in the Chlorophyta, such as monophyly of the Ulvophyceae (the class in which the order Bryopsidales is currently classified).ResultsBoth DNAs are circular and lack a large inverted repeat. The cpDNA of B. plumosa is 106,859 bp long and contains 115 unique genes. A 13 kb region was identified with several freestanding open reading frames (ORFs) of putative bacterial origin, including a large ORF (>8 kb) closely related to bacterial rhs-family genes. The cpDNA of T. expeditiones is 105,200 bp long and contains 125 unique genes. As in B. plumosa, several regions were identified with ORFs of possible bacterial origin, including genes involved in mobile functions (transposases, integrases, phage/plasmid DNA primases), and ORFs showing close similarity with bacterial DNA methyltransferases. The cpDNA of B. hypnoides differs from that of B. plumosa mainly in the presence of long intergenic spacers, and a large tRNA region. Chloroplast phylogenomic analyses were largely inconclusive with respect to monophyly of the Ulvophyceae, and the relationship of the Bryopsidales within the Chlorophyta.ConclusionsThe cpDNAs of B. plumosa and T. expeditiones are amongst the smallest and most gene dense chloroplast genomes in the core Chlorophyta. The presence of bacterial genes, including genes typically found in mobile elements, suggest that these have been acquired through horizontal gene transfer, which may have been facilitated by the occurrence of obligate intracellular bacteria in these siphonous algae.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1418-3) contains supplementary material, which is available to authorized users.

Highlights

Species of Bryopsidales form ecologically important components of seaweed communities worldwide
Results and discussion chloroplast DNA (cpDNA) assembly, size and organization For both Bryopsis plumosa and Tydemania expeditiones, assemblies yielded a single cpDNA sequence, which could be closed into a circle by an overlap of more than 300 base pairs
The circular cpDNAs of B. plumosa (Figure 2) and T. expeditiones (Figure 3) consist of 106,859 bp and 105,200 bp, respectively. This is smaller than most published cpDNAs of free-living species of core Chlorophyta, but similar to those found in Pedinomonas minor (98 kb), Marvania geminata (108 kb), Pseudochloris wilhelmii (110 kb), and Planctonema lauterbornii (114 kb) [9,19,22]

Summary

Introduction

Species of Bryopsidales form ecologically important components of seaweed communities worldwide. The 153.4 kb cpDNA of B. hypnoides differs in several aspects from the two other species of Ulvophyceae It does not feature a quadripartite architecture, and it includes 10 tRNA genes that are not present in any other green algal cpDNA. Another peculiarity of the B. hypnoides cpDNA is the presence of multimeric forms of the cpDNA, including monomers, dimers, trimers, tetramers, and higher-order multimers, which were detected by pulsed-field gel electrophoresis and Southern blot methods [13]. Apart from completely sequenced cpDNAs, partial chloroplast genome data in the Bryopsidales has long been available for Codium fragile [14] and Caulerpa sertularoides [15] through Southern hybridization analysis of restriction fragments. In addition partial DNA sequence data is available for Caulerpa filiformis [16]

Methods

Results

Conclusion