Molecular markers of the mitochondrial genomes of Isopoda and implications on the phylogeny of Peracarida (Crustacea: Malacostraca) [Elektronische Ressource] / Fabian Kilpert

Fabian Kilpert

Informations

• Publié par: rheinische_friedrich-wilhelms-universitat_bonn
• Publié le: 01 janvier 2010
• Nombre de lectures: 21
• Langue: Deutsch
• Poids de l'ouvrage: 12 Mo

Extrait

MOLECULAR MARKERS OF THE MITOCHONDRIAL GENOMES OF ISOPODA
AND IMPLICATIONS ON THE PHYLOGENY
OF PERACARIDA (CRUSTACEA: MALACOSTRACA)





D i s s e r t a t i o n
Zur Erlangung des Grades
Doktor der Naturwissenschaften (Dr. rer. nat.)


Institut für Evolutionsbiologie und Zooökologie
Mathematisch-Naturwissenschaftliche Fakultät
Rheinische Friedrich-Wilhelms-Universität




Fabian Kilpert
aus Lübeck




Bonn, Dezember 2009



Diese Arbeit wurde mit Genehmigung der Mathematisch-Naturwissenschaftlichen Fakultät
der Rheinischen Friedrich-Wilhelms-Universität Bonn angefertigt.





















Erstgutachter: Prof. Dr. Thomas Bartolomaeus
Zweitgutachter: Privat-Dozent Dr. Lars Podsiadlowski

Tag der mündlichen Prüfung: 19. April 2010

Abgabe: Dezember 2009
Erscheinungsjahr: 2010

II



















Eidesstattliche Erklärung

Hiermit erkläre ich, dass ich die vorliegende Arbeit ohne unzulässige Hilfe Dritter und
ohne Benutzung anderer als der angegebenen Hilfsmittel angefertigt habe. Die aus
anderen Quellen direkt oder indirekt übernommenen Daten und Konzepte sind unter
Angabe der Quelle gekennzeichnet.

Die Arbeit wurde bisher weder im In- noch im Ausland in gleicher oder ähnlicher Form
einer anderen Prüfungsbehörde vorgelegt.


Bonn, Dezember 2009


Fabian Kilpert


III The dissertation is based on following publications:

Chapter 2: Kilpert F, Podsiadlowski L: The complete mitochondrial genome of the
common sea slater, Ligia oceanica (Crustacea, Isopoda) bears a novel gene order and
unusual control region features. BMC Genomics 2006, 7:241

Chapter 3: Kilpert F, Podsiadlowski L: The Australian fresh water isopod
(Eophreatoicidea: Isopoda) allows insights into the early mitogenomic evolution of
isopods. Comp. Biochem. Phys. D; doi: 10.1016/j.cbd.2009.09.003

Chapter 4: Kilpert F, Held C, Podsiadlowski L: Rearrangements of the mitochondrial
genome of Isopoda and implications on the phylogeny of Peracarida. Gen. Biol. Evol. –
submitted.

Chapter 5: Kilpert F, Podsiadlowski L: The mitochondrial genome of the Japanese
skeleton shrimp Caprella mutica (Amphipoda: Caprellidea) reveals a unique gene order
and shared apomorphic translocations with Gammaridea. Mitochon. DNA – submitted.



Contributions of the listed authors:

Chapter 2: FK did the majority of laboratory work. LP was the initiator and the
supervisor of the work. Manuscript writing was done by FK and LP in equal parts.

Chapter 3: FK did the majority of laboratory work and manuscript writing. LP was
supervisor and helped in writing the manuscript.

Chapter 4: FK did the majority of laboratory work and manuscript writing. CH provided
the Glyptonotus specimen and helped in manuscript writing. LP was supervisor and
helped in writing the manuscript.

Chapter 5: FK did the majority of laboratory work and manuscript writing. TB was co-
supervisor. LP was supervisor and helped in writing the manuscript.

Contributions of further persons are mentioned in the acknowledgement section of
respective chapters.



IV Contents


1. General introduction 6

The complete mitochondrial genome of the common sea slater, 16 2.
Ligia oceanica (Crustacea, Isopoda) bears a novel gene order
and unusual control region features

The Australian fresh water isopod (Eophreatoicidea: Isopoda) 41 3.
allows insights into the early mitogenomic evolution of isopods

4. Rearrangements of the mitochondrial genome of Isopoda and 59
implication on the phylogeny of Peracarida

5. The mitochondrial genome of the Japanese skeleton shrimp 89
Caprella mutica (Amphipoda: Caprellidea) reveals a unique
gene order and shared apomorphic translocations with
Gammaridea

6. Insights from the mitochondrial genome of Leucon nasica 104
(Cumacea) – Implications for peracarid phylogeny

Concluding discussion 109 7.

8. Summary 115

Zusammenfassung 116 9.

10. Collected references 117

Appendix 129 11.

12. Curriculum vitae 172

Danksagung 175 13.

V 1. General introduction

1.1 The mitochondrion
The mitochondrion is a specialized, independent compartment and of particular
importance to the eukaryotic cell. A double membrane encloses the organelle and
allows it to process several vital metabolic pathways separate from the cytoplasm
(Brand, 1997; Seyffert, 2003). In this regard it also takes a key role in a number of
crucial cell processes, e.g. aging (Wei, 1998), apoptosis (Kroemer et al., 1998), diseases
(Graeber and Muller, 1998). The mitochondrion is mainly well-known for being the site
of oxidative phosphorylation. Electrons are transferred through a series of protein
complexes (electron transport chain), located in the inner mitochondrial membrane, to
an electron acceptor, which is in most animals oxygen (O ). The energy released during 2
that redox reaction is used to generate a potential of protons across the inner
mitochondrial membrane, which is on its part used as an energy source for the enzyme
ATP synthase to phosphorylate adenosine diphosphate (ADP) to adenonsine
triphosphate (ATP). The molecule ATP serves as a general energy supply for the cell.
For this reason, at least one or several mitochondria are present in almost every
respiring animal cell, dependent on the required amount of energy. It is conspicuous that
mitochondria reproduce by binary fission only and are generally inherited by the female
germ line (maternal inheritance). Mitochondria also contain their own genome, referred
to as the mitochondrial DNA (mtDNA), which encodes protein subunits of the electron
transport chain. The mtDNA also uses a derived genetic code to specify amino acids
(Osawa et al., 1990; Osawa et al., 1992).
The commonly accepted endosymbiont theory (Sagan, 1967) supposes that
mitochondria are derived from prokaryotes (alpha-proteobacteria), which established a
symbiotic relationship with the primitive eukaryotic cell. Eukaryotes bearing
mitochondria are assumed to exist at least since the Palaeoprotozoic (2,500 to 1,600
mya) (Knoll et al., 2006), the age when the oxygen level in the earth’s atmosphere
significantly rose by photosynthesis. Since then the mitochondrial (mt) genome has
evolved alongside with the nuclear genome. Consequently, the evolutionary history
should be reflected in the mtDNA of successive organisms (Saccone et al., 1999).
6 1. General introduction
1.2 The mitochondrial genome
The genomes of alpha-proteobacteria (e.g. of Rickettsia prowazekii) revealed a high
similarity to the mtDNA of eukaryotes — a strong indication for their common origin.
Early mitochondria certainly possessed the complete genetic information of their
bacterial ancestors. In the course of gradual transformation to a cell organelle, however,
the gene content was significantly reduced. Some genes were simply lost, as they were
dispensable in an endosymbiontic environment, but most of the genes were successively
transferred to the nuclear genome (Adams and Palmer, 2003; Martin et al., 2001). This
general trend is well traced by the declining number of mt genes in several protists,
rhodophytes, and chlorophytes (Seyffert, 2003).
In mt genomes of bilaterian animals (Bilateria) the gene content has been reduced to 37
genes (2 rRNA genes, 13 protein subunit genes, 22 tRNA genes). The encoded
polypeptides are all subunits of the protein complexes, which are part of the
mitochondrial oxidative phosphorylation system (Taanman, 1999). The rRNAs are part
of the mt protein synthesizing machinery. Apart from genes, also one non-coding region
is found in the mtDNA. Bearing controlling elements for replication and transcription, it
is called the mitochondrial control region (CR). Even though mitochondria may
maintain their own system of DNA replication, transcription, mRNA processing and
protein translation, they strongly rely on proteins and RNAs from the cytoplasm as well.

The mtDNA usually has a size of 15-20 kb and is organized as a ring-shaped double-
helix. The larger mt genomes that are known up to now, only result from duplications of
parts of the genome and not from variations of the gene content. Gene losses, in most
cases of tRNA genes, were occasionally reported from certain lineages, e.g. nematodes,
cnidarians, bivalves (Boore, 1999), and chaetognathes (Helfenbein et al., 2004). The mt
nucleotide sequence is generally evolving faster than in sequences from the nuclear
genome.
The highly economical organization of the mt genome is striking: Unlike in nuclear
DNA no introns and nearly no non-coding intergenic sequences exi