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Publications - Nicole Dubilier

2018 Bang C, Dagan T, Deines P, Dubilier N, Duschl WJ, Fraune S, Hentschel U, Hirt H, Hülter N, Lachnit T, Picazo D, Pita L, Pogoreutz C, Rädecker N, Saad MM, Schmitz RA, Schulenburg H, Voolstra CR, Weiland-Bräuer N, Ziegler M, Bosch TCG (2018). Metaorganisms in extreme environments: do microbes play a role in organismal adaptation?. Zoology. In press. DOI:

Bergin C, Wentrup C, Brewig N, Blazejak A, Erséus C, Giere O, Schmid M, de Wit P, Dubilier N (2018). Acquisition of a novel sulfur-oxidizing symbiont in the gutless marine worm Inanidrilus exumae. Applied and Environmental Microbiology (posted online Jan 12, 2018). doi:10.1128/AEM.02267-17


2017 Dubilier N (2017). High tide for marine microbes. Cell 169: 771.

Tavormina PL, Kellermann MY, Antony CP, Tocheva E, Dalleska N, Jensen AJ, Valentine DL, Hinrichs K-U, Jensen G, Dubilier N, Orphan VJ (2017). Starvation and recovery in the deep-sea methanotroph Methyloprofundus sedimenti. Molecular Microbiology 103: 242-252. doi: 10.1111/mmi.13553

2016 Zimmermann J, Wentrup C, Sadowski M, Blazejak A, Gruber‐Vodicka H, Kleiner M, Ott J, Cronholm B, De Wit P, Erséus C, Dubilier N. 2016. Closely coupled evolutionary history of ecto‐and endosymbionts from two distantly‐related animal phyla. Molecular Ecology. Early View, March 15, 2016. doi:10.1111/mec.13554
  Schimak MP, Kleiner M, Wetzel S, Liebeke M, Dubilier N, Fuchs BM (2016). MiL-FISH: Multilabeled oligonucleotides for fluorescence in situ hybridization improve visualization of bacterial cells. Applied and Environmental Microbiology Early View, October 2015, 82 (1): 62-70. doi:10.1128/aem.02776-15
2015Kleiner M, Wentrup C, Holler C, Lavik G, Harder J, Lott C, Littmann S, Kuypers MMM, Dubilier N (2015). Use of carbon monoxide and hydrogen by a bacteria-animal symbiosis from seagrass sediments. Environmental Microbiology 17(12): 5023-5035. doi:10.1111/1462-2920.12912
Sayavedra L, Kleiner M, Ponnudurai R, Wetzel S, Pelletier E, Barbe V, Shoguchi E, Satoh N, Reusch TBH, Rosenstiel P, Schilhabel MB, Becher D, Schweder T, Markert S, Dubilier N, Petersen JM (2015). Abundant toxin-related genes in the genomes of beneficial symbionts from deep-sea hydrothermal vent mussels. eLife 4. doi:
Dubilier N, McFall-Ngai M, Zhao L. 2015. Create a global microbiome effort. Nature 526: 631-634
2014Petersen JM, Dubilier N (2014) Gene swapping in the dead zone. eLife 3:e04600.
Wentrup C, Wendeberg A, Schimak M, Borowski C, Dubilier N (2014) Forever competent: Deep-sea bivalves are colonized by their chemosynthetic symbionts throughout their lifetime. Environmental Microbiology 16(12): 3699–3713. DOI: 10.1111/1462-2920.12597
Zimmermann J, Lott C, Weber M, Ramette A, Bright M, Dubilier N, Petersen JM (2014) Dual symbiosis with co-occurring sulfur-oxidizing symbionts in vestimentiferan tubeworms from a Mediterranean hydrothermal vent. Environmental Microbiology 16(12): 3638–3656. DOI: 10.1111/1462-2920.12427
Beinart RA, Nyholm SV, Dubilier N, Girguis PR (2014) Intracellular Oceanospirillales inhabit the gills of the hydrothermal vent snail Alviniconcha with chemosynthetic, γ-Proteobacterial symbionts. Environmental Microbiology Reports 6(6): 656–664. DOI: 10.1111/1758-2229.12183
Jan C, Petersen JM, Werner J, Teeling H, Huang S, Glöckner FO, Golyshina OV, Dubilier N, Golyshin PN, Jebbar M and Cambon-Bonavita M-A (2014) The gill chamber epibiosis of deep-sea shrimp Rimicaris exoculata: an in-depth metagenomic investigation and discovery of Zetaproteobacteria. Environmental Microbiology 16: 2723–2738. 10.1111/1462-2920.1240
Russel JA, Dubilier N and Rudgers JA (2014) Nature's microbiome. Molecular Ecology 23(6): 1225–1237. DOI: 10.1111/mec.12676
2013McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Loso T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013). Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences. 110(9): 3229-3236. doi: 10.1073/pnas.1218525110
Raggi L, Schubotz F, Hinrichs K-U, Dubilier N, Petersen JM (2013). Bacterial symbionts of Bathymodiolus mussels and Escarpia tubeworms from Chapopote, an asphalt seep in the southern Gulf of Mexico. Environmental Microbiology. Advance online publication. doi:10.1111/1462-2920.12051
Wentrup C, Wendeberg A, Huang JY, Borowski C, Dubilier N (2013). Shift from widespread symbiont infection of different host tissues to spatially restricted colonization of gill cells in early life stages of hydrothermal vent mussels. ISME Journal. 7: 1244-1247. doi:10.1038/ismej.2013.5
Kleiner M, Young JC, Shah M, VerBerkmoes NC, Dubilier N (2013). Metaproteomics reveals abundant transposase expression in mutualistic endosymbionts. mBio. 4(3): e00223-13. doi: 10.1128/mBio.00223-13
2012Kleiner M, Wentrup C, Lott C, Teeling H, Wetzel S, Young J, Chang YJ, Shah M, VerBerkmoes NC, Zarzycki J, Fuchs G, Markert S, Hempel K, Voigt B, Becher D, Liebeke M, Lalk M, Albrecht D, Hecker M, Schweder T, Dubilier N (2012). Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use. Proceedings of the National Academy of Sciences. 109(19): 7148-7149. doi: 10.1073/pnas.1121198109 (open access)
Kleiner M, Petersen JM, Dubilier N (2012) Convergent and divergent evolution of metabolism in sulfur-oxidizing symbionts and the role of horizontal gene transfer. Current Opinion in Microbiology 15:621-631.
Petersen JM, Wentrup C, Verna C, Knittel K, Dubilier N (2012) Origins and evolutionary flexibility of chemosynthetic symbionts from deep-sea animals. Biological Bulletin 223:123-137
van der Heijden K, Petersen JM, Dubilier N, Borowski C (2012). Genetic connectivity between North and South Mid-Atlantic Ridge chemosynthetic bivalves and their symbionts. PLoS One 7(7): e39994. doi:10.1371/journal.pone.0039994
Kellermann MY, Schubotz F, Elvert M, Lipp JS, Birgel D, Prieto-Mollar X, Dubilier N, Hinrichs K-U (2012). Symbiont-host relationships in chemosynthetic mussels: A comprehensive lipid biomarker study. Organic Geochemistry 43, 112-124. doi:10.1016/j.orggeochem.2011.10.005
Wendeberg A, Zielinski FU, Borowski C, Dubilier N (2012). Expression patterns of mRNAs for methanotrophy and thiotrophy in symbionts of the hydrothermal vent mussel Bathymodiolus puteoserpentis. ISME Journal 6, 104-112. doi:10.1038/ismej.2011.81
Gros O, Elisabeth NH, Gustave SDD, Caro A, Dubilier N (2012). Plasticity of symbiont acquisition throughout the life cycle of the shallow-water tropical lucinid Codakia orbiculata (Mollusca: Bivalvia). Environmental Microbiology 14, 1584-1595, doi:10.1111/j.1462-2920.2012.02748.x
2011Petersen JM, Zielinski FU, Pape T, Seifert R, Moraru C, Amann R, Hourdez S, Girguis PR, Wankel SD, Barbe V, Pelletier E, Fink D, Borowski C, Bach W, Dubilier N (2011). Hydrogen is an energy source for hydrothermal vent symbioses. Nature 476, 176–180. doi:10.1038/nature10325
Hugler M, Petersen JM, Dubilier N, Imhoff JF, Sievert SM (2011). Pathways of carbon and energy metabolism of the epibiotic community associated with the deep-sea hydrothermal vent shrimp Rimicaris exoculata. PLoS One 6. doi:e1601810.1371/journal.pone.0016018
Kleiner M, Woyke T, Ruehland C, Dubilier N (2011).The Olavius algarvensis metagenome revisited: lessons learned from the analysis of the low diversity microbial consortium of a gutless marine worm. In: Handbook of Molecular Microbial Ecology II; Metagenomics in Different Habitats. Ed: de Bruijn FJ. Wiley/Blackwell.
Zielinski FU, Gennerich H, Borowski C, Wenzhöfer F, Dubilier N. (2011) In situ measurements of hydrogen sulfide, oxygen, and temperature in diffuse fluids of an ultramafic-hosted hydrothermal vent field (Logatchev, 14°45′N, Mid-Atlantic Ridge): Implications for chemosymbiotic bathymodiolin mussels. Geochemistry Geophysics Geosystems 12, Q0AE04. doi:10.1029/2011GC003632.
2010Petersen JM, Ramette A, Lott C, Cambon Bonavita M-A, Zbinden M, Dubilier N (2010). Dual symbiosis of the vent shrimp Rimicaris exoculata with filamentous gamma- and epsilonproteobacteria at four Mid-Atlantic Ridge hydrothermal vent fields. Environmental Microbiology 12, 2204-2218. doi:10.1111/j.1462-2920.2009.02129.x
Ruehland C, Dubilier N (2010). Gamma- and epsilonproteobacterial ectosymbionts of a shallow-water marine worm are related to deep-sea hydrothermal vent ectosymbionts. Environmental Microbiology 12, 2312–2326. doi: 10.1111/j.1462-2920.2010.02256.x
Verna C, Ramette A, Wiklund H, Dahlgren TG, Glover AG, Gaill F and Dubilier N (2010). High symbiont diversity in the bone-eating worm Osedax mucofloris from shallow whale-falls in the North Atlantic. Environmental Microbiology 12, 2355–2370. doi: 10.1111/j.1462-2920.2010.02299.x
Zielinski F, Dubilier N (2010) Der Eukaryoten-Zellkern als ökologische Nische für Bakterien. BioSpektrum01-10 16 p.12-15
2009Zielinski FU, Pernthaler A, Duperron S, Raggi L, Giere O, Borowski C, Dubilier N (2009). Widespread occurrence of an intranuclear bacterial parasite in vent and seep bathymodiolin mussels. Environmental Microbiology 11, 1150-1167. doi: 10.1111/j.1462-2920.2008.01847.x
Petersen JM and Dubilier N (2009). Symbiotic methane oxidizers. In: Handbook of Hydrocarbon and Lipid Microbiology. Ed: Kenneth M. Timmis. Springer Verlag, Heidelberg, doi:10.1007/978-3-540-77587-4_145
Petersen JM and Dubilier N (2009). Methanotrophic symbioses in marine invertebrates. Environmental Microbiology Reports (2009) 1(5), 319–335, doi:10.1111/j.1758-2229.2009.00081.x
2008Dubilier N, Bergin C, Lott C. 2008. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nature Reviews Microbiology 6: 725-740
Lösekann T, Robador A, Niemann H, Knittel K, Boetius A, Dubilier N. 2008. Endosymbioses between bacteria and deep-sea siboglinid tubeworms from an Arctic cold seep (Haakon Mosby Mud Volcano, Barents Sea). Environ. Microbiol. 10: 3237-3254
Ruehland C, Blazejak A, Lott C, Loy A, Erséus C, Dubilier N. 2008. Multiple bacterial symbionts in two species of co-occurring gutless marine worms from Mediterranean sea grass sediments. Environ. Microbiol. 10: 3404-3416
Martínez-García M, Stief P, Díaz-Valdés M, Wanner G, Ramos-Esplá A, Dubilier N, and Antón J. 2008. Ammonia-oxidizing Crenarchaeota and nitrification inside the tissue of a colonial ascidian. Environ. Microbiol. 10: 2991-3001
2007Dubilier N. 2007. The searchlight and the bucket of microbial ecology. Environ. Microbiol. 9, 2-3.
Duperron S, Sibuet M, MacGregor BJ, Kuypers MMM, Fisher CR, Dubilier N. 2007. Diversity, relative abundance, and metabolic potential of bacterial endosymbionts in three Bathymodiolus mussel species from cold seeps in the Gulf of Mexico. Environ. Microbiol. 9: 1423-1438
Haase KM, Petersen S, Koschinsky A, Seifert R, Devey C, Dubilier N, Fretzdorff S, Garbe-Schönberg D, German CR, Giere O, Keir R, Kuever J, Lackschewitz K, Mawick J, Marbler H, Melchert B, Mertens C, Paulick H, Perner M, Peters M, Sander S, Schmale O, Stecher J, Strauss H, Süling J, Stöber U, Walter M, Weber S, Westernströer U, Yoerger D, Zielinski F (2007) Young volcanism and related hydrothermal activity at 5°S on the slow-spreading southern Mid-Atlantic Ridge. Geochemistry Geophysics Geosystems 8: Vol. 8, Q11002, DOI 10.1029/2006GC001509
Musat N, Giere O, Gieseke A, Thiermann F, Amann R, Dubilier N. 2007. Molecular and morphological characterization of the association between bacterial endosymbionts and the marine nematode Astomonema sp. from the Bahamas. Environ. Microbiol. 9: 1345-1353.
Pernice M, Wetzel S, Gros O, Boucher-Rodoni R, Dubilier N. 2007. Enigmatic dual symbiosis in the excretory organ of Nautilus macromphalus (Cephalopoda: Nautiloidea). Proc. R. Soc. B. 274: 1143-1152.
Pradillon F, Schmidt A, Peplies J, Dubilier N. 2007. Species identification of marine invertebrate early stages by whole – larvae in situ hybridisation of 18S ribosomal RNA. Mar. Ecol. Prog. Ser. 333: 103-116.
2006Woyke T, Teeling H, Ivanova NN, Richter M, Hunteman M, Gloeckner FO, Boffelli D, Barry KW, Shapiro HJ, Mussmann M, Bergin C, Ruehland C, Amann R, Anderson IJ, Szeto E, Kyrpides NC, Markowitz VM, Rubin EM, Dubilier N. 2006. Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443: 950-955.
Da Silva SG, Gillan DC, Dubilier N, De Ridder, C. 2006. Characterization by 16S rRNA gene analysis and in situ hybridization of bacteria living in the hindgut of a deposit-feeding echinoid (Echinodermata). J. Mar. Biol. Assoc. UK 86:1209-1213.
Ruehland C, Bergin C, Lott C, Dubilier N. 2006 Darmlose marine Würmer: Symbiosen mit mikrobiellen Konsortien. BIOspektrum 06:600-602
Blazejak, A., Kuever, J., Erséus, C., Amann, R., Dubilier, N. (2006). Phylogeny of 16S rRNA, ribulose 1,5-bisphosphate carboxylase/oxygenase, and adenosine 5’-phosphosulfate reductase genes from gamma- and alphaproteobacterial symbionts in gutless marine worms (Oligochaeta) from Bermuda and Bahamas. Appl. Environ. Microbiol. 72: 5527-5536.
Dubilier, N., Blazejak, A., Ruehland, C. (2006). Symbioses between bacteria and gutless marine oligochaetes. In: J. Overmann (ed) Molecular Basis of Symbiosis. Springer Verlag, New York. Pp 251-275.
Duperron, S., Bergin, C., Zielinski, F., Pernthaler, A., Dando, P., McKiness, Z.P., DeChaine, E., Cavanaugh, C.M., Dubilier, N.(2006). A dual symbiosis shared by two mussel species, Bathymodiolus azoricus and B. puteoserpentis (Bivalvia: Mytilidae), from hydrothermal vents along the northern Mid-Atlantic Ridge. Environ. Microbiol. 8: 1441-1447.
Musat, N., Werner, U., Kolb, S., Dodenhof, T., Knittel, K., van Beusekom, J.E.E., Dubilier, N., Amann, R. (2006). Microbial community structure of sandy intertidal sediments in the North Sea, Sylt-Rømø Basin, Wadden Sea. Syst. Appl. Microbiol. 29: 333-348.
2005Blazejak, A., Erséus, C., Amann, R., Dubilier, N. 2005. Coexistence of bacterial sulfide-oxidizers, sulfate-reducers, and spirochetes in a gutless worm (Oligochaeta) from the Peru margin. Appl. Environ. Microbiol. 71: 1553-1561
Duperron, S., Nadalig, T., Caprais, J.-C., Sibuet, M., Fiala-Médioni, A., Amann, R., Dubilier, N. 2005. Dual symbiosis in a Bathymodiolus sp. mussel from a methane seep on the Gabon continental margin (Southeast Atlantic): 16S rRNA phylogeny and distribution of the symbionts in gills. Appl. Environ. Microbiol. 71: 1694-1700
Urakawa, H., Dubilier, N., Fujiwara, Y., Cunningham, D.E., Kojima, S., Stahl, D.A. 2005. Hydrothermal vent gastropods from the same family (Provannidae) harbour gamma - and epsilon-proteobacterial endosymbionts. Environ. Microbiol. 7: 750-754.
de Beer, D., Wenzhöfer, F., Ferdelman, T.G., Boehme, S.E., Huettel, M., van Beusekom, J.E.E., Böttcher, M.E., Musat, N., Dubilier, N. 2005. Transport and mineralization rates in North Sea sandy intertidal sediments, Sylt-Rømø Basin, Wadden Sea. Limnol. Oceanogr. 50: 113-127
2004Gillan, D.C. & Dubilier, N. 2004. Novel epibiotic Thiothrix bacterium on a marine amphipod. Appl. Environ. Microbiol. 70: 3772-3775
Dubilier, N. 2004. Multiple bacterial endosymbionts in gutless marine worms: competitors or partners? Nova Acta Leopoldina NF 88: 107-112
2003Schramm, A., Davidson, S.K., Dodsworth, J.A., Drake, H.L., Stahl, D.A., Dubilier, N. 2003. Acidovorax-like endosymbionts in the nephridia of earthworms. Environ. Microbiol. 5: 804-809
2002Borowski, C., Giere, O., Krieger, J., Amann, R., Dubilier, N. 2002. New aspects of the symbiosis in the provannid snail Ifremeria nautilei from the North Fiji Back Arc Basin. Cahiers de Biologie Marine 43: 321-324
Dubilier, N., Mülders, C., Blazejak, A. 2002. Eine ungewöhnliche Symbiose in einem darmlosen Meereswurm. BIOforum 3: 127-129
2001Dubilier, N., Mülders, C., Ferdelman, T., de Beer, D., Hentschke, A., Klein M., Wagner, M., Erséus, C., Thiermann, F., Krieger, J., Giere, O., and Amann, R. Endosymbiotic sulfate-reducing and sulfide-oxidizing bacteria in a gutless marine worm (Oligochaeta, Anneldia). 2001. Nature 411: 298-302.
2000Krieger, J. Giere, O., and Dubilier, N. Localization of RubisCO and sulfur in endosymbiotic bacteria of the gutless marine oligochaete Inanidrilus leukodermatus (Annelida). 2000. Mar. Biol. 137: 239-244
1999Dubilier, N., Amann, R., Erséus, C., Muyzer, G., Park, S., Giere, O., and Cavanaugh, C.M. 1999. Phylogenetic diversity of bacterial endosymbionts in the gutless marine oligochaete Olavius loisae (Annelida). Mar. Ecol. Prog. Ser. 178: 271-280.
Giere, O., Preusse, J.-H., and Dubilier, N. 1999. Tubificoides benedii (Tubificidae, Oligochaeta) - a pioneer in hypoxic and sulfidic environments. An overview of adaptive pathways. Hydrobiologia 406: 235-241.
1998Dubilier N., Windoffer R., Giere O. 1998. Ultrastructure and stable carbon isotope composition of the hydrothermal vent mussels Bathymodiolus brevior and B. sp. affinis brevior from the North Fiji Basin, western Pacific. Mar. Ecol. Prog. Ser. 165: 187-193.
1997Dubilier, N., Grieshaber, M.K. and Giere, O. 1997. Ultrastructure and anaerobic metabolism of mitochondria in the marine oligochaete Tubificoides benedii. Mar. Biol. 127: 637-645.
1996Krueger, D., Dubilier, N., and Cavanaugh, C.M. 1996. Molecular characterization of chemoautotrophic bacterial symbionts in Solemya occidentalis (Mollusca, Bivalvia). Mar. Biol. 126: 55-64.
1995Dubilier, N., Giere, O., Distel, D.L., and Cavanaugh, C.M. 1995. Chemoautotrophic bacterial symbionts in a gutless marine worm (Oligochaeta, Annelida): Phylogenetic 16S rRNA sequence analysis and in situ hybridization. Appl. Environ. Microbiol. 61: 2346-2350.
Dubilier, N., Giere, O. and Grieshaber, M. 1995. Morphological and ecophysiological adaptations of the marine oligochaete Tubificoides benedii to sulfidic sediments. Amer. Zool. 35: 163-173.
1994Dubilier, N., Giere, O. and Grieshaber, M. 1994. Concomitant effects of sulfide and hypoxia on the aerobic metabolism of the marine oligochaete Tubificoides benedii. J. Exp. Zool. 269: 287-297.
1988Dubilier, N. 1988. H2S - A settlement cue or a toxic substance for Capitella sp. l larvae? Biol. Bull. 174: 30-38.
Giere, O., Rhode, B. and Dubilier, N. 1988. Structural peculiarities of the body wall of Tubificoides benedii (Oligochaeta) and possible relations to its life in sulphidic sediments. Zoomorphology 108: 29-39.
1986Dubilier, N. 1986. Association of filamentous epibacteria with Tubificoides benedii (Oligochaeta: Annelida). Mar. Biol. 92: 285-288.
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