Microbiota – host interactions at the base of the metazoan tree

This project addresses in a comparative approach the presence, establishment and functional consequences of microbiota in two basal metazoan animals, the comb jelly Mnemiopsis leidyi (Ctenophora) and the cnidarian Aurelia aurita. Both occur in the same ocean habitat, and share the same food, facilitating an inter-phylum comparison by controlling for environment and bacterial colonizer pool. The project aims to compare the role of environment, external disturbance and challenge by opportunistic pathogens for the specificity and functioning of associated microbiota. First, we will analyze and evaluate the relative effects of environment versus host genotypes on the establishment and the composition of the respective microbiota. Second, we will evaluate the role of the microbiota for host fitness correlated functions including successful invasion (Mnemiopsis) and life cycle decisions (Aurelia and Mnemiopsis). To this end, animals will be made germ-free, and experimentally controlled recolonization with defined microbial communities compared to controls will allow us to evaluate diverse fitness-correlated effects in the laboratory. A third key objective is to study the ways of inter-kingdom communication in establishing a specific microbiota in both hosts, including host immunity and bacterial communication. In particular, we address mechanisms of signal exchange between host and microbiota, including quorum quenching strategies (interference with bacterial cell-cell communication). Finally, we will assess how associated microbiota is involved in host defense targeting opportunistic pathogens. The proposed comparative approach will allow insights into general and specific hostmicrobe interactions and (fitness-correlated) functions of the associated microbiota. Depending on the host gene and receptor repertoire we expect different mechanisms and end-points of host-microbe interaction among both phyla. The project will contribute to the CRC by broadening the comparative approach at the base of the metazoan tree, allowing deep evolutionary insight into ancient hostmicrobial interactions.


Dr. Anna Roik

Postdoctoral Researcher
Kiel University Institute for General Microbiology



Construction and Screening of Marine Metagenomic Large Insert Libraries.

Weiland-Bräuer N, Langfeldt D, Schmitz R A (2017); Methods Mol Biol., 1539:23-42. doi: 10.1007/978-1-4939-6691-2_3


Year-Long Monitoring of Physico-Chemical and Biological Variables Provide a Comparative Baseline of Coral Reef Functioning in the Central Red Sea.

Roik A, Röthig T, Roder C, Ziegler M, Kremb S G, Voolstra C R (2016); PLoS ONE, 11(11):e0163939. doi: 10.1371/journal.pone.0163939

Biophysical and Population Genetic Models Predict the Presence of “Phantom” Stepping Stones Connecting Mid-Atlantic Ridge Vent Ecosystems.

Breusing C, Biastoch A, Drews A, Metaxas A, Jollivet D, Vrijenhoek R C, Bayer T, Melzner F, Sayavedra L, Petersen J M, Dubilier N, Schilhabel M B, Rosenstiel P, Reusch T B (2016); Curr Biol., 26(17):2257-67. doi: 10.1016/j.cub.2016.06.062

Combination of bottom up 2D-LC-MS and semi-top-down GelFree-LC-MS enhances coverage of proteome and low molecular weight short open reading frame encoded peptides of the archaeon Methanosarcina mazei

Cassidy L , Prasse D, Linke D, Schmitz RA, Tholey A (2016); J Proteome Res. doi:10.1021/acs.jproteome.6b00569

Widespread formation of alternative 3′ UTR isoforms via transcription termination in archaea

Dar D, Prasse D, Schmitz R A, Sorek R (2016); Nature Microbiology, 1(16143). doi: 10.1038/nmicrobiol.2016.143

Host-parasite coevolution-rapid reciprocal adaptation and its genetic basis.

Kurtz J, Schulenburg H, Reusch T B (2016); Zoology (Jena), 119(4):241-3. doi: 10.1016/j.zool.2016.06.011

Highly effective inhibition of biofilm formation by the first 1 metagenome-derived AI-2 quenching enzyme.

Weiland-Bräuer N, Kisch M, Pinnow N, Liese A, Schmitz R A (2016); Front Microbiol., 7:1098. doi: 10.3389/fmicb.2016.01098

Antimicrobial and anti-Quorum Sensing activities of selected medicinal plants of Ethiopia: Implication for development of potent antimicrobial agents.

Bacha K, Tariku Y, Gebreyesus F, Zerihun S, Mohammed A, Weiland-Bräuer N, Schmitz R A, Mulat M (2016); BMC Microbiol., 16(1):139. doi: 10.1186/s12866-016-0765-9

Quorum quenching–Stören friede zwischenbakterieller Beziehungen.

Schmitz-Streit R A, Weiland-Bräuer N (2016); BioSpektrum, 22(4):362-364. doi: 10.1007/s12268-016-0698-8

Spatial and seasonal reef calcification in corals and calcareous crusts in the central Red Sea.

Roik A, Roder C, Röthig T, Voolstra C R (2016); Coral Reefs, 35(2):681–693. doi: 10.1007/s00338-015-1383-y

Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea.

Ziegler M, Roik A, Porter A, Zubier K, Mudarris M S, Ormond R, Voolstra C R (2016), Marine Pollution Bulletin, 105(2):629-640. doi: 10.1016/j.marpolbul.2015.12.045

It’s the economy, stupid! Projecting the fate of fish populations using ecological-economic modeling.

Quaas M, Reusch T B H, Schmidt J O, Tahvonen O, Voss R (2016); Global Change Biology, 22:264–270. doi: 10.1111/gcb.13060

Restructuring of epibacterial communities on Fucus vesiculosus forma mytili in response to elevated pCO2 and increased temperature levels.

Mensch B, Neulinger S C, Graiff A, Pansch A, Künzel S, Fischer M A, Schmitz R A (2016); Frontiers in Microbiology. doi: 10.3389/fmicb.2016.00434

Long-term salinity tolerance is accompanied by major restructuring of the coral bacterial microbiome.

Röthig T, Ochsenkühn M A, Roik A, van der Merwe R, Voolstra C R (2016); Mol Ecol., 25:1308–1323. doi: 10.1111/mec.13567

Methanosarcina flavescens sp. nov., a methanogenic archaeon isolated from a full-scale anaerobic digester.

Kern T, Fischer M A, Deppenmeier U, Schmitz R A, Rother M (2016); Int J Syst Evol Microbiol., 66:1533-1538.  doi: 10.1099/ijsem.0.000894

Influence of mesoscale eddies on the distribution of nitrous oxide in the eastern tropical South Pacific.

Arévalo-Martínez D L, Kock A, Löscher C R, Schmitz R A, Stramma L, Bange H W (2016); Biogeosciences, 13:1105-1118. doi:10.5194/bg-13-1105-2016

The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea.

Olsen J L, Rouzé P, Verhelst B, Lin Y-C, Bayer T, Collén J, Dattolo E, De Paoli E, Dittami S, Maumus F, Michel G, Kersting A, Lauritano C, Lohaus R, Töpel M, Tonon T, Vanneste K, Amirebrahimi M, Brakel J, Boström C, Chovatia M, Grimwood J, Jenkins J, Jüterbock A, Mraz A, Stam W T, Tice H, Bornberg-Bauer E, Green P, Pearson G, Procaccini G, Duarte C, Schmutz J, Reusch T B H, Van de Peer Y (2016); Nature, 530:331-335. doi: 10.1038/nature16548

Transcriptome profiling of immune tissues reveals habitat-specific gene expression between lake and river sticklebacks.

Huang Y, Chain F J, Panchal M, Eizaguirre C, Kalbe M, Lenz T L, Samonte I E, Stoll M, Bornberg-Bauer E, Reusch T B H, Milinski M, Feulner P G (2016); Mol Ecol., 25(4):943-58. doi: 10.1111/mec.13520


First description of small proteins encoded by spRNAs in Methanosarcina mazei strain Gö1.

Prasse D, Thomsen J, De Santis R, Muntel J, Becher D, Schmitz R A (2015); Biochimie.; 117:138-48. doi: 10.1016/j.biochi.2015.04.007

Composition of Bacterial Communities Associated with Aurelia aurita Changes with Compartment, Life Stage, and Population.

Weiland-Bräuer N, Neulinger S C, Pinnow N, Künzel S, Baines J F, Schmitz R A (2015); Appl Environ Microbiol., 81(17):6038-6052.  doi: 10.1128/AEM.01601-15

Interactions of gelatinous zooplankton within marine food webs.

Jaspers C, Acuña J L, Brodeur R D (2015); J Plankton Res, 37(5):985-988. doi: 10.1093/plankt/fbv068

Dynamic changes of the luminal and mucosa-associated gut microbiota during and after antibiotic therapy with paromomycin.

Heinsen F A, Knecht H, Neulinger S C, Schmitz R A, Knecht C, Kühbacher T, Rosenstiel P C, Schreiber S, Friedrichs A K, Ott S J (2015); Gut Microbes., 6(4):243-54. doi: 10.1080/19490976.2015.1062959.

Archaea associated with human surfaces: not to be underestimated.

Bang C, Schmitz R A (2015); FEMS Microbiology reviews., 39(5):631-48. doi: 10.1093/femsre/fuv010

Reproduction rates under variable food conditions and starvation in Mnemiopsis leidyi: significance for the invasion success of a ctenophore.

Jaspers C, Møller L F, Kiørboe T (2015); J Plankton Res, 37(5):1011-1018. doi: 10.1093/plankt/fbv017

Captive rearing of the deep-sea coral Eguchipsammia fistula from the Red Sea demonstrates remarkable physiological plasticity.

Roik A, Röthig T, Roder C, Müller P J, Voolstra C R (2015); PeerJ, 3:e734. doi: 10.7717/peerj.734

Elevating the predatory effect: Sensory-scanning foraging strategy by the lobate ctenophore Mnemiopsis leidyi.

Colin S P, MacPherson R, Gemmell B, Costello J H, Sutherland K, Jaspers C (2014); Limnology and Oceanography, 60(1):100-109. doi: 10.1002/lno.10007


Carbon content of Mnemiopsis leidyi eggs and specific egg production rates in northern Europe.

Jaspers C, Costello J H, Colin S P (2014); J Plankton Res, 37(1):11-15. doi: 10.1093/plankt/fbu102

Health- and disease-associated species clusters in complex natural biofilms determine the innate immune response in oral epithelial cells during biofilm maturation.

Langfeldt D, Neulinger S C, Stiesch M, Stumpp N, Bang C, Schmitz R A, Eberhard J (2014); FEMS Microbiology, 360(2):137-43. doi: 10.1111/1574-6968.12596

Mechanisms behind the metabolic flexibility of an invasive comb jelly.

Augustine S, Jaspers C, Kooijman S, Carlotti F, Poggiale J C, Freitas V, van der Veer H, van Walraven L (2014); Journal of Sea Research, 94:156–165. doi: 10.1016/j.seares.2014.09.005

Facets of diazotrophy
in the oxygen minimum zone waters off Peru.

Löscher  C R, Großkopf T, Desai F D, Gill D, Schunck H, Croot P L , Schlosser C, 
Neulinger S C, Pinnow N, Lavik G, Kuypers M M M, LaRoche J, Schmitz R A (2014); ISME Journal, 8(11):2180-92. doi: 10.1038/ismej.2014.71

Biofilm formation of mucosa-associated methanoarchaeal strains.

Bang C, Ehlers C, Orell A, Prasse D, Spinner M, Gorb S N, Albers S V, Schmitz R A (2014); 
Frontiers Microbiol., 5:353. doi: 10.3389/fmicb.2014.00353

The intestinal archaea Methanosphaera stadtmanae and Methanobrevibacter smithii activate human dendritic cells.

Bang C, Weidenbach K, Gutsmann T, Heine H, Schmitz R A (2014); PlosOne, 9(6):e99411. doi: 10.1371/journal.pone.0099411

Effects of β-lactam antibiotics and fluoroquinolones on human gut microbiota in relation to Clostridium difficile associated diarrhea.

Knecht H, Neulinger S C, Heinsen F A, Knecht C, Schilhabel A, Schmitz R A, Zimmermann A, dos Santos V M, Ferrer M, Rosenstiel P C, Schreiber S, Friedrichs A K, Ott S J (2014); PLoS One., 9(2):e89417. doi: 10.1371/journal.pone.0089417

Thioredoxin targets fundamental processes in a methane-producing
 archaeon, Methanocaldococcus jannaschii.

Susanti D, Wong J H, Vensel W H, Loganathan U, DeSantis R, Schmitz R A, Balsera M, Buchanan B B, Mukhopadhyay B (2014); Proc Natl Acad Sci USA, 111(7):2608-13. doi: 10.1073/pnas.1324240111

Composition of microbial supragingival biofilms in young healthy adults in correlation to experimentally induced gingivitis.

Langfeldt D, Neulinger S C, Heuer W, Staufenbiel I, Sven Künzel S, Baines J F, Eberhard J, Schmitz R A (2014); PLosOne, 9(2):e87449. doi: 10.1371/journal.pone.0087449

Small regulatory RNAs in Archaea.

Babski J, Maier L K, Heyer R, Jaschinski K, Prasse D, Jäger D, Randau L, Schmitz R A, Marchfelder A, Soppa J (2014); RNA Biol., 11(5):484-93. doi: 10.4161/rna.28452


Environmental constraints of the invasive Mnemiopsis leidyi in Scandinavian waters

Haraldsson M, Jaspers C, Tiselius P, Aksnes D L, Andersen T, Titelman J (2013); Limnology and Oceanography, 58(2):763. doi: 10.4319/lo.2013.58.2.0763

Low-level inflammation in the prevalent oral disease gingivitis induces surrogate markers of atherosclerosis in young healthy individuals. An interventional study.

Eberhard J , Grote K, Luchtefeld M, Heuer W, Schuett H, Divchev D, Scherer R, Schmitz R A, Langfeldt D, Stumpp N, Staufenbiel I, Schieffer B, Stiesch M (2013); PLOS one, 8(2):e55265.  doi: 10.1371/journal.pone.0055265

Regulatory RNAs in archaea: first target identification in Methanoarchaea.

Prasse D, Ehlers C, Backofen R, Schmitz R A (2013); Biochem Soc Trans., 41(1):344-9. doi: 10.1042/BST20120280

Genome-wide patterns of standing genetic variation in a marine population of three-spined sticklebacks.

Feulner P G, Chain F J, Panchal M, Eizaguirre C, Kalbe M, Lenz T L, Mundry M, Samonte I E, Stoll M, Milinski M, Reusch T B H, Bornberg-Bauer E (2013); Mol Ecol., 22(3):635-49. doi: 10.1111/j.1365-294X.2012.05680.x

Seasonal dynamics of early life stages of invasive and native ctenophores give clues to invasion and bloom potential in the Baltic Sea.

Jaspers C, Haraldsson M, Lombard F, Bolte S, Kiørboe T (2013); J Plankton Res, 35(3):582-594. doi: 10.1093/plankt/fbt001


An archaeal
sRNA targeting cis- and trans-encoded mRNAs via two distinct domains.

Jäger D, Pernitzsch S R, Richter A, Backofen R, Sharma C M, Schmitz R A (2012); Nucleic Acids
Res., 40:10964-79. doi: 10.1093/nar/gks847

N2 fixation rates in the Atlantic Ocean have been severely underestimated.

Großkopf, T, W. Mohr, T. Baustian, H. Schunck, D. Gill, M.M.M. Kuypers, G. Lavik, R.A. Schmitz, 
D.W.R. Wallace, J. LaRoche (2012); 
Nature, 488(7411):361-4.

Adaptive evolution of a key phytoplankton species
to ocean acidification.

Lohbeck K T, Riebesell U, Reusch T B H (2012); Nature Geosci., 5:346-351. doi: 10.1038/ngeo1441

Hosts are ahead in a marine hostparasite
coevolutionary arms race: innate immune system adaptation in pipefish Syngnathus typhle
against Vibrio phylotypes.

Roth O, Keller I, Landis S H, Salzburger W, Reusch T B H (2012); Evolution, 66(8):2528–2539. doi: 10.1111/j.1558-5646.2012.01614.x

Environmental constraints of the invasive Mnemiopsis leidyi in Scandinavian waters

Haraldsson M, Jaspers C, Tiselius P, Aksnes D L, Andersen T, Titelman J (2012); Limnology and Oceanography, 58(1):37–48. doi: 10.4319/lo.2013.58.1.0037

Ctenophore population recruits entirely through larval reproduction in the central Baltic Sea.

Jaspers C, Haraldsson M, Bolte S, Reusch T B, Thygesen U H, Kiørboe T (2012); Biol Lett., 8(5):809-12. doi: 10.1098/rsbl.2012.0163

Small RNAs for defence and regulation in archaea.

Marchfelder A, Fischer S, Brendel J, Stoll B, Maier L K, Jäger D, Prasse D, Plagens A, Schmitz R A, Randau L (2012); Extremophiles., 16(5):685-96. doi: 10.1007/s00792-012-0469-5

Effects of Antimicrobial Peptides on Methanogenic Archaea.

Bang C, Schilhabel A, Weidenbach K, Kopp A, Goldmann T, Gutsmann T, Schmitz R A (2012); Antimicrobial Agents and Chemotherapy, 56(8):4123-30. doi:

Occurrence, inter-annual variability and zooplankton-predation impact of the invasive ctenophore Mnemiopsis leidyi and the native jellyfish Aurelia aurita in Limfjorden (Denmark) in 2010 and 2011.

Riisgård H U, Jaspers C, Serre S, Lundgreen K (2012); BioInvasions Records, 1(3):145-159. doi: 10.3391/bir.2012.1.3.01


Transcriptomic resilience to global warming in the seagrass Zostera marina, a marine
foundation species.

Franssen S U, Gu J, Bergmann N, Winters G, Klostermeier U C, Rosenstiel P, Bornberg-Bauer E, Reusch T B (2011); Proc Natl Acad Sci U S A., 108(48):19276-81. doi: 10.1073/pnas.1107680108

Long-term effects of grazing and global warming on the composition and carrying capacity of graminoid marshes for moulting geese in east Greenland.

Madsen J, Jaspers C, Tamstorf M, Mortensen C E, Rigét F (2011); Ambio., 40(6):638-49. doi: 10.1007/s13280-011-0170-4

Salinity gradient of the Baltic Sea limits the reproduction and population expansion of the newly invaded comb jelly Mnemiopsis leidyi.

Jaspers C, Møller L F, Kiørboe T (2011); PLoS One., 6(8):e24065. doi: 10.1371/journal.pone.0024065

BpiB05, a novel metagenome-derived hydrolase acting on N-acylhomoserine lactones.

Bijtenhoorn P, Schipper C, Hornung C, Quitschau M, Grond S, Weiland N, Streit W R (2011); J Biotechnol., 155(1):86-94. doi: 10.1016/j.jbiotec.2010.12.016

rRNA-based profiling of bacteria in the axilla of healthy males suggests right-left asymmetry in bacterial activity.

Egert M, Schmidt I, Höhne H-M, Lachnit T, Schmitz R , Breves R (2011); FEMS Microbiology Ecology, 77:146-153. doi: 10.1111/j.1574-6941.2011.01097.x

Epibacterial community patterns on marine macroalgae are host-specific but temporally variable.

Lachnit T, Meske D, Wahl M, Harder T, Schmitz R A (2011); Environmental Microbiology, 13(3):655-65. doi: 10.1111/j.1462-2920.2010.02371.x

Production and fate of copepod fecal pellets across the Southern Indian Ocean.

Møller E F,Andersen Borg C M, Jónasdóttir S H, Satapoomin S, Jaspers C, Gissel Nielsen T (2011); Mar Biol, 158(3):677–688. doi: 10.1007/s00227-010-1591-5

The invasive ctenophore Mnemiopsis leidyi poses no direct threat to Baltic cod eggs and larvae.

Jaspers C, Titelman J, Hansson L J, Haraldsson M, Røllike Ditlefsen C (2011); Limnology and Oceanography, 56(2):431-439. doi: 10.4319/lo.2011.56.2.0431


Construction and screening of marine metagenomic libraries.

Weiland N, Löscher C, Metzger R, Schmitz R (2010); Methods Mol Biol., 668:51-65. doi: 10.1007/978-1-60761-823-2_3


Deep sequencing
analysis of the Methanosarcina mazei Gö1 transcriptome in response to nitrogen availability.

Jäger D, Sharma C M, Thomsen J, Ehlers C, Vogel J, Schmitz R A (2009); Proc.
Nat. Acad. Sci. USA, 106(51):21878-21882. doi: 10.1073/pnas.0909051106

Metazooplankton distribution across the Southern Indian Ocean with emphasis on the role of Larvaceans.

Jaspers C, Gissel Nielsen T, Carstensen J, Hopcroft R R, Møller E F (2009); J Plankton Res., 31(5):525–540. doi: 10.1093/plankt/fbp002


Genetic variation in MHC class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks.

Wegner K M, Kalbe M, Rauch G, Kurtz J, Schaschl H, Reusch T B H (2006); Mol Ecol., 15(4):1153-1164. doi: 10.1111/j.1365-294X.2006.02855.x


Unique mechanistic
features of post translational regulation of glutamine synthetase activity in Methanosarcina mazei in
response to nitrogen availability.

Ehlers C, Weidenbach K, Veit K, Forchhammer K and Schmitz R A (2005); Mol. Microbiol., 55:1841-1854. doi: 10.1111/j.1365-2958.2005.04511.x

Ecosystem recovery after climatic extremes
enhanced by genotypic diversity.

Reusch T B H, Ehlers A, Hämmerli A, Worm B (2005); Proc Natl Acad Sci USA, 102:2826-2831. doi: 10.1073/pnas.0500008102


Metagenomics – the key to the uncultured microbes.

Streit W R, Schmitz R A (2004); Opin. Microbiol., 7:492–498. doi: 10.1016/j.mib.2004.08.002


Parasite selection for immunogenetic

Wegner K M, Kalbe M, Kurtz J, Reusch T B H, Milinski M (2003); Science, 301:1343. doi: 10.1126/science.1088293


Female sticklebacks count alleles in a
strategy of sexual selection explaining MHC polymorphism.

Reusch T B H, Häberli M A, Aeschlimann P B, Milinski M (2001); Nature, 414(6861):300-302, doi: 10.1038/35104547


Screening of environmental 
DNA libraries for the presence of genes conferring lipolytic activity to Escherichia coli.

Henne A, Schmitz R A, Bömeke M, Gottschalk G, Daniel R (2000); Appl. Environ.
 Microbiol., 66:3113-3116. doi: 10.1128/AEM.66.7.3113-3116.2000