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Our Research


The major topics currently under investigation in our laboratory are:

Plastids and mitochondria were once free-living prokaryotes – at the time of endosymbiosis they possessed all genes necessary for that free-living lifestyle. But today, organelle genomes are very highly reduced relative to the genomes of their free-living cousins. Chloroplast genomes encode about 5–10% as many proteins as free-living cyanobacteria, mitochondrial genomes encode about 1–3% as many proteins as free-living alpha-proteobacteria. But both organelles contain roughly as many proteins as their free-living prokaryotic relatives. To explain this, there is something called endosymbiotic gene transfer: During evolution, organelles relinquished many genes to the chromosomes of their host, but they also learned to reimport the nuclear-encoded products of transferred genes. Endosymbiotic gene transfer is much, much more widespread than is generally assumed. The thrust of our earlier work on this topic involved comparisons of selected genes from specific biochemical pathways. Currently, we are using genome-wide phylogenies of genes in sequenced genomes to obtain some quantitative estimates for the fraction of genes that eukaryotes acquired from organelles - both during primary and secondary endosymbioses. Of course, we are also interested not only in the "how much", but also in the "how" and "why" of endosymbiotic gene transfer, not to mention the more pressing question of why organelles have retained genomes at all.


Some papers on this topic are:

  • Martin W, Stoebe B, Goremykin V, Hansmann S, Hasegawa M, Kowallik KV (1998) Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393:162–165.
  • Rujan T, Martin W (2001) How many genes in Arabidopsis come from cyanobacteria? An estimate from 386 protein phylogenies. Trends in Genetics 17:113–120. 
  • Race HL, Herrmann RG, Martin W (1999) Why have organelles retained genomes? Trends in Genetics 15:364–370. 
  • Henze K, Martin W (2001) How are mitochondrial genes transferred to the nucleus? Trends in Genetics 17:383–387. 
  • Martin W (1999) Mosaic bacterial chromosomes – A challenge en route to a tree of genomes. BioEssays 21:99–104. 
  • Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: How much, what happens and why? Plant Physiol. 118:9–17 
  • Deane JA, Fraunholz M, SuV, Maier U-G, Martin W, Durnford DG, McFadden GI (2000): Evidence for nucleomorph to host nucleus gene transfer: light-harvesting complex proteins from cryptomonads and chlorarachniophytes. Protist 151:239–252. 
  • Henze K, Schnarrenberger C, Martin W (2001) Endosymbiotic gene transfer: A special case of horizontal gene transfer germane to endosymbiosis, the origins of organelles and the origins of eukaryotes. In Horizontal Gene Transfer. Syvanen M, Kado C (eds). Academic Press, London. pp. 343–352. 
  • Martin W (1996) Is something wrong with the tree of life? BioEssays 18:523–527. 
  • Henze K, Badr A, Wettern M, Cerff R and Martin W (1995) A nuclear gene of eubacterial origin in Euglena gracilis reflects cryptic endosymbioses during protist evolution. Proc. Natl. Acad. Sci. USA 92:9122–9126. 
  • Martin W, Brinkmann H, Savona C, Cerff R (1993) Evidence for a chimaeric nature of nuclear genomes: Eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes. Proc. Natl. Acad. Sci. USA 90:8692–8696.

There are many groups of eukaryotes known that live in anaerobic environments. They do not possess textbook-like mitochondria: Some possess anaerobic mitochondria, some possess hydrogenosomes (hydrogen-producing mitochondria that usually lack a genome), and some possess no organelles of ATP-synthesis at all. The classical 'endosymbiont hypothesis' fails to account for the origin of these anaerobic organelles and their anaerobic biochemstry. We have put forward an alternative model for the origins of organelles, one that accounts both for oxygen-dependent and for anaerobic ATP-synthesis in eukaryotes (the 'hydrogen hypothesis'). We are currently testing the predictions of that model by investigating the enzymes of energy metabolism in two groups of eukaryotes that possess hydrogenosomes and in the photosynthetic protists Euglena gracilis, which has an unusual wax-ester fermentation in its facultatively anaerobic mitochondria. This work is currently flanked by proteom work (mass-spectrometry microsequencing of proteins from isolated organelles), by EST projects, and by DNA-microarray studies to examine gene expression profiles.


Some papers on this topic are:

  • Martin W, Müller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 392:37–41. 
  • Embley TM, Martin W (1998) A hydrogen-producing mitochondrion. Nature 396:517–519. 
  • Martin W (2000) A powerhouse divided. Science 287:1219. 
  • Rotte C, Martin W (2001) Endosymbiosis does not explain the origin of the nucleus. Nature Cell Biol. 8:E173–174. 
  • Rotte C, Stejskal F, Zhu G, Keithly JS, Martin W (2001) Pyruvate:NADP+ oxidoreductase from the mitochondrion of Euglena gracilis and from the apicomplexan Cryptosporidium parvum: A fusion of pyruvate:ferredoxin oxidoreductase and NADPH-cytochrome P450 reductase. Mol. Biol. Evol. 18:710–720. 
  • Rotte C, Henze K, Müller M, Martin W (2000) Origins of hydrogenosomes and mitochondria. Curr. Opin. Microbiol. 3:481–486. 
  • Martin W (2000) Primitive anaerobic protozoa: The wrong host for mitochondria and hydrogenosomes? Microbiology 146:1021–1022. 
  • Martin W (1999) A briefly argued case that mitochondria and plastids are descendants of endosymbionts, but that the nuclear compartment is not. Proc. Roy. Soc. Lond. B. 266:1387–1395. 
  • Müller M, Martin W (1999) The genome of Rickettsia prowazekii and some thoughts on the origins of mitochondria and hydrogenosomes. BioEssays 21:377–381. 
  • Dooijes D, Chaves I, Kieft R, Martin W, Borst P (2000) Conservation outside the order Kinetoplastida of base J as a constituent of nuclear but not nucleolar DNA in Euglena gracilis. Nucl. Acids Res. 28:3017–3021. 
  • Martin W, Hoffmeister M, Rotte C, Henze K (2001) An overview of endosymbiotic models for the origins of eukaryotes, their ATP-producing organelles (mitochondria and hydrogenosomes), and their heterotrophic lifestyle. Biol. Chem. 382:1521–1539.

Using a straightforward gene-for-gene approach, we have studied the evolutionary history of (all of) the enzymes of the Calvin cycle, glycolysis, gluconeogenesis, the citric acid cycle in higher plants. We have also studied the evolution of some other pathways, including the mevanolate and deoxyxylulose-5-phosphate pathways of isoprene biosynthesis. We have found that all of the nuclear-encoded enzymes involved in central carbon metabolism in higher plants are more similar to their eubacterial homologues than they are to their archaebacterial homologues, the single exception being enolase. Surprisingly, this is true not only for the enzymes localized in organelles, but also for the enzymes localized in the eukaryotic cytosol. Much more surprisingly, also in eukaryotes that lack organelles altogether, the enzymes of primary carbohydrate metabolism are more similar to their eubacterial than to their archaebacterial homologues. Overall, it looks to us as if eukaryotes acquired not only their organelles through endosymbiosis, but also the enzymatic backbone of their heterotrophic lifesytle.


Some papers on this topic are:

  • Lange BM, Rujan T, Martin W, Croteau R (2000) Isoprenoid biosynthesis: The evolution of two ancient and distinct pathways across genomes. Proc. Natl. Acad. Sci. USA 97:13172–13177. 
  • Schnarrenberger C, Martin W (2002) Evolution of the enzymes of the citric acid cycle and the glyoxylate cycle of higher plants: A case study of endosymbiotic gene transfer. Eur. J. Biochem. 269:868–883. 
  • Krepinsky K, Plaumann M, Martin W, Schnarrenberger C (2001) Purification and cloning of chloroplast 6-phosphogluconate dehydrogenase from spinach: Cyanobacterial genes for chloroplast and cytosolic isoenzymes encoded in eukaryotic chromosomes. Eur. J. Biochem. 268: 2678–2686. 
  • Hannaert V, Brinkmann H, Nowitzki U, Lee JA, Albert M-A, Sensen C, Gaasterland T, Müller M, Michels P, Martin W (2000) Enolase from Trypanosoma brucei, from the amitochondriate protist Mastigamoeba balamuthi, and from the chloroplast and cytosol of Euglena gracilis: Pieces in the evolutionary puzzle of the eukaryotic glycolytic pathway. Mol. Biol. Evol. 17:989–1000. 
  • Liaud M-F, Lichtlé C, Apt K, Martin W, Cerff R (2000) Compartment-specific isoforms of TPI and GAPDH are imported into diatom mitochondria as a fusion protein: Evidence in favor of a mitochondrial origin of the eukaryotic glycolytic pathway. Mol. Biol. Evol. 17: 213–223. 
  • Martin W, Scheibe R, Schnarrenberger C (2000) The Calvin cycle and its regulation. In Advances in Photosynthesis Vol. 9. R.C. Leegood, T.D. Sharkey, S. von Caemmerer (eds). Kluwer Academic Publishers. pp. 9–51. 
  • Flechner A, Gross W, Martin W, Schnarrenberger C (1999) Chloroplast class I and class II aldolases are bifunctional for fructose-1,6-bisphosphate and sedoheptulose-1,7-bisphosphate cleavage in the Calvin cycle. FEBS Lett. 447:200–202. 
  • Nowitzki U, Flechner A, Kellermann J, Hasegawa M, Schnarrenberger C, Martin W (1998) Eubacterial origin of eukaryotic nuclear genes for chloroplast and cytosolic glucose-6-phosphate isomerase: Sampling eubacterial gene diversity in eukaryotic chromosomes through symbiosis. Gene 214:205–213. 
  • Meyer-Gauen G, Herbrand H, Pahnke J, Cerff R, Martin W (1998) Gene structure, expression in Escherichia coli and biochemical properties of the NAD+-dependent glyceraldehyde-3-phosphate dehydrogenase from Pinus sylvestris chloroplasts. Gene 209:167–174. 
  • Martin W, Schnarrenberger C (1997) The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: A case study of functional redundancy in ancient pathways through endosymbiosis. Curr. Genet. 32:1–18.

In recent years, we have focussed a bit on the evolution and biology of organelles, but we still maintain an active interest in phylogeny. In addition to keeping track of the gene content and the phylogeny of chloroplast genomes we have had a interest in the question of whether the Gnetales – an unusual group of gymnosperms with very angiosperm-like characters – are the sisters of angiosperms or not (they aren't). In recent work together with friends in Cologne, we're also investigating some aspects of cereal domestication.


Some papers on these topics are:

  • Hansen A, Hansmann S, Samigullin T, Antonov A, Martin W (1999) Gnetum and the angiosperms: Molecular evidence that their shared morphological characters are convergent, rather than homologous. Mol. Biol. Evol. 16:1006–1009. 
  • Goremykin VV, Bobrova VK, Pahnke J, Troitsky AV, Antonov AS, Martin W (1996) Noncoding sequences from the slowly evolving chloroplast inverted repeat in addition to rbcL data do not support gnetalean affinities of angiosperms. Mol. Biol. Evol. 13:383–396. 
  • Samigullin TH, Martin W, Troitsky AV, Antonov AS (1999) Molecular data from the chloroplast rpoC1 gene suggest a deep and distinct dichotomy of contemporary spermatophytes into two monophylums: gymnosperms (including Gnetales) and angiosperms. J. Mol. Evol. 49:310–315. 
  • Adachi J, Waddell P, Martin W, Hasegawa M (2000) Plastid phylogeny and a model of amino acid substitutions of proteins encoded in chloroplast DNA. J. Mol. Evol. 50:348–358. 
  • Goremykin V, Hansmann S, Martin W (1997) Evolutionary analysis of 58 proteins encoded in six completely sequenced chloroplast genomes: Revised molecular estimates of two seed plant divergence times. Pl. Syst. Evol. 206:337–351. 
  • Martin W, Stoebe B, Goremykin V, Hansmann S, Hasegawa M, Kowallik KV (1998) Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393:162–165. 
  • Stoebe B, Hansmann S, Goremykin V, Kowallik KV, Martin W (1999) Proteins encoded in sequenced chloroplast genomes. In: Advances in Plant Molecular Systematics. Eds. Hollingsworth C, et al. Francis and Taylor, Andover. pp. 327–352. 
  • Stoebe B, Martin W, Kowallik KV (1998) Distribution and nomenclature of protein-coding genes in 12 sequenced chloroplast genomes. Plant Mol. Biol. Reptr. 16:243–255. 
  • Samigullin TH, Valiejo-Roman KM, Troitsky AV, Bobrova VK, Filin VR, Martin W, Antonov AS (1998) Sequence of rDNA internal spacers from the chloroplast DNA of 26 bryophytes: Properties and phylogenetic utility. FEBS Lett. 422:47–51. 
  • Martin W, Gierl A, Saedler H (1989) Angiosperm origins. Nature 342:132. 
  • Martin W, Gierl A, Saedler H (1989) Molecular evidence for pre-Cretaceous angiosperm origins. Nature 339:46–48. 
  • Martin W, Salamini F (2000) Biodiversity and natural history: A meeting at the gene. EMBO Reports 1:208–210.

Der endosymbiotische Ursprung der Plastiden führte zur Vererbarkeit der Photosynthese in Eukaryoten. Es gibt allerdings auch Fälle, in denen eukaryotische Photosynthese über nicht erbliche, symbiotische Assoziationen stattfindet, wie im Falle der küstenbewohnenden Nacktschnecken aus der Gruppe der Sacoglossa. Während einige Schneckenarten wahllos unterschiedliche Algen fressen und verdauen, wählen manche selektiv ihre Nahrungsquelle (bestimmte siphonale Algenarten, wie Acetabularia oder Vaucheria) und lagern selektiv nur die Plastiden ein. Bemerkenswert an diesem System ist, dass die Kleptoplasten (gestohlene Plastiden) im Zytosol von Epithelzellen eingelagert werden, welche den Verdauungstrakt aufbauen. Kleptoplasten können von manchen Schnecken Wochen bis Monate funktionell eingelagert werden und in den Schneckenzellen Sonnenenergie ernten und für biologische Zwecke einsetzen. Bis heute bleiben die spannendsten Fragen bei diesen Nacktschnecken: a) Wie können ihre Plastiden so lange aktiv bleiben? b) Warum können nur wenige der mehr als 300 bekannten Sacoglossenarten Kleptoplastiden für mehrere Wochen funktionell einlagern? und c) Wie überhaupt funktioniert die Selektion und Aufnahme der Kleptoplastiden in den Epithelzellen des Schneckendarms? Die Zusammenarbeit mit den Arbeitsgruppen Wägele (Bonn), Jahns (Düsseldorf) und Nickelsen (München) erlaubt einen multidisziplinären Ansatz zur Klärung dieser Fragen.


Weiterführende Literatur

de Vries J, Christa G, Gould SB: Plastid survival in the cytosol of animal cells. Trends Plant Sci 19:347–350 (2014). pdf

Christa G, de Vries, Jahns P, Gould SB: Switching off photosynthesis: The dark side of sacoglossan slugs. Commun Integr Biol 7:e28029 (2014). pdf

Schmitt V, Händeler K, Gunkel S, Escande ML, Menzel D, Gould SB, Martin WF, Wägele H: Chloroplast incorporation and long-term photosynthetic performance through the life cycle in laboratory cultures of Elysia timida (Sacoglossa, Heterobranchia). Front Zool 11:5 (2014). pdf

Christa G, Zimorski V, Woehle C, Tielens AGM, Wägele H, Martin WF, Gould SB: Plastid-bearing sea slugs fix CO2 in the light but do not require photosynthesis to survive. Proc R Soc Lond B 281:20132493 (2014). pdf 

de Vries J, Habicht J, Woehle C, Huang C, Christa G, Wägele H, Nickelsen J, Martin WF, Gould SB: Is ftsH the key to plastid longevity in sacoglossan slugs? Genome Biol Evol 5:2540–2548 (2013). pdf

Martin WF, Hazkani-Covo E, Shavit-Grievink L, Schmitt V, Händeler K, Gould SB, Landan G, Graur D, Dagan T: Gene transfers from organelles to the nucleus. How much, what happens, and why none in ElysiaEndocytobiosis Cell Res 23:16–20 (2012). pdf

Wagele H, Deusch O, Handeler K, Martin R, Schmitt V, Christa G, Pinzger B, Gould SB, Dagan T, Klussmann-Kolb A, Martin W: Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobranchus ocellatus does not entail lateral transfer of algal nuclear genes. Mol Biol Evol 28:699–706 (2011). pdf

At the moment we are particularly interested in endosymbiosis and the origin of eukaryotes. This is an important topic that goes back 100 years. I translated Mereschkowsky's seminal 1905 paper on this topic from German into English, it is a very worthwhile read and can be downloaded here. A review summarizing the majors issues that we currently recognize at the forefront of the field of eukaryote origins is available here. Sometimes I get requests for various figures that have appeared in my papers, click here to view and download from the current gallery. For whatever reason, people often ask me "Where did the nucleus come from?" – my critique of existing models and my own alternative model can be found in a paper published in 2005 (PDF).


Experimental Tools

Our experimental tools in the laboratory are:

  • Standard biochemistry (enzyme purification, kinetic studies, etc.),
  • Standard molecular biology (cloning, sequencing, gene expression analysis, PCR),
  • Analysis of active enzymes overexpressed in E. coli or other systems,
  • Cell fractionation and organelle isolation (for proteomics and enzyme localization),
  • Molecular evolution at the computer (phylogeny, gene and genome analysis, bioinformatics).
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