The dinoflagellates Durinskia baltica and Kryptoperidinium foliaceum retain functionally overlapping mitochondria from two evolutionarily distinct lineages

Behzad Imanian,Patrick J Keeling

doi:10.1186/1471-2148-7-172

Abstract

BackgroundThe dinoflagellates Durinskia baltica and Kryptoperidinium foliaceum are distinguished by the presence of a tertiary plastid derived from a diatom endosymbiont. The diatom is fully integrated with the host cell cycle and is so altered in structure as to be difficult to recognize it as a diatom, and yet it retains a number of features normally lost in tertiary and secondary endosymbionts, most notably mitochondria. The dinoflagellate host is also reported to retain mitochondrion-like structures, making these cells unique in retaining two evolutionarily distinct mitochondria. This redundancy raises the question of whether the organelles share any functions in common or have distributed functions between them.ResultsWe show that both host and endosymbiont mitochondrial genomes encode genes for electron transport proteins. We have characterized cytochrome c oxidase 1 (cox1), cytochrome oxidase 2 (cox2), cytochrome oxidase 3 (cox3), cytochrome b (cob), and large subunit of ribosomal RNA (LSUrRNA) of endosymbiont mitochondrial ancestry, and cox1 and cob of host mitochondrial ancestry. We show that all genes are transcribed and that those ascribed to the host mitochondrial genome are extensively edited at the RNA level, as expected for a dinoflagellate mitochondrion-encoded gene. We also found evidence for extensive recombination in the host mitochondrial genes and that recombination products are also transcribed, as expected for a dinoflagellate.ConclusionDurinskia baltica and K. foliaceum retain two mitochondria from evolutionarily distinct lineages, and the functions of these organelles are at least partially overlapping, since both express genes for proteins in electron transport.

Highlights

The dinoflagellates Durinskia baltica and Kryptoperidinium foliaceum are distinguished by the presence of a tertiary plastid derived from a diatom endosymbiont
A short fragment of cox1 could be amplified from DNA, probably due to the presence of long type II introns such as those found in diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana and the endosymbiont of K. foliaceum [9], so the remainder was recovered from RNA by RT-PCR
Diatom-derived genes for cox1, cox3 and cob are already known from K. foliaceum [9], so to complement the D. baltica data we amplified the K. foliaceum cox2 and large subunit ribosomal RNA (LSUrRNA)

Summary

Introduction

The dinoflagellates Durinskia baltica and Kryptoperidinium foliaceum are distinguished by the presence of a tertiary plastid derived from a diatom endosymbiont. The dinoflagellate host is reported to retain mitochondrion-like structures, making these cells unique in retaining two evolutionarily distinct mitochondria This redundancy raises the question of whether the organelles share any functions in common or have distributed functions between them. Whereas mitochondria originated once and have apparently never been lost [3,4,5], plastids have spread between eukaryotic lineages several times in events referred to as secondary and tertiary endosymbioses. Even in the most severely reduced, anaerobic parasites which lack oxidative phosphorylation, highly reduced organelles called mitosomes and hydrogenosomes are found [3,4,5] Some of these have no direct role in energy metabolism, but iron-sulfur cluster biosynthesis is a common function [5,7,8]. These relict organelles suggest mitochondria are resistant to outright loss, raising questions about why mitochondria appear to be one of the more dispensable features of algae taken up during secondary and tertiary endosymbiosis events

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