B1

Host-microbe cross talk in the early metazoan taxa Porifera and anthozoan Cnidaria

The term “metaorganism” was coined in recognition of the fact that in the environment, all multicellular hosts (animals, plants) associate with microorganisms (1). The concept has profound impacts on our understanding of ecology which seeks to understand the interactions between organisms and between organisms and their environment. There is a growing awareness that such microbial communities may fulfill many essential functions, from nutrition to development and defense against pathogens. This proposal B1 seeks to investigate host-microbe interactions in two early-branching metazoans, sponges and cnidarians. It was shown that sponges and cnidarians are colonized by specific bacterial communities, which is suggestive of highly selective pressures by the host animal. Recent genome projects of sponges and cnidarians have identified potential receptors, signal transduction cascades, and effector molecules involved in epithelial defence. In this proposal, we hypothesize that there is an intimate interaction between bacterial community and the host immune system and that the bacterial colonizers will contribute to host fitness. Neither aspect has been investigated in detail in the proposed experimental models. To elucidate these interactions, we will focus on two main aims in Nematostella and two selected sponge species in a comparative approach: 1. Host mechanisms involved in recognition and establishment of specific bacterial colonization. 2. Bacterial function and localization during development. Together, these insights, which will be derived from in vitro and in vivo studies, will unveil ancient mechanisms controlling host-microbe recognition, function and homeostasis during development. Because these phyla have preserved much of the genetic complexity of the common metazoan ancestor it promises to be highly informative to discover evolutionarily conserved mechanisms controlling host-microbe interactions.

Researchers

Martin Jahn

PhD Candidate, Associated Junior Researcher
GEOMAR - Helmholtz Centre for Ocean Research Kiel

Laura Baldassarre

PhD Candidate, Associated Junior Researcher
Kiel University Zoological Institute

Publications

2016

Emerging Sponge Models of Animal-Microbe Symbioses.

Pita L, Fraune S, Hentschel U (2016); Front Microbiol., 7:2102. doi: 10.3389/fmicb.2016.02102

Potential of marine natural products against drug-resistant fungal, viral, and parasitic infections.

Abdelmohsen U R, Balasubramanian S, Oelschlaeger T A, Grkovic T, Pham N B, Quinn R J, Hentschel U (2016); Lancet Infect Dis., pii:S1473-3099(16)30323-1. doi: 10.1016/S1473-3099(16)30323-1

Antifungal potential of marine natural products.

El-Hossary E M, Cheng C, Hamed M M, El-Sayed Hamed A N, Ohlsen K, Hentschel U, Abdelmohsen U R (2016);
Eur J Med Chem., 126:631-651. doi: 10.1016/j.ejmech.2016.11.022

An Enrichment of CRISPR and Other Defense-Related Features in Marine Sponge-Associated Microbial Metagenomes.

Horn H, Slaby B M, Jahn M T, Bayer K, Moitinho-Silva L, Förster F, Abdelmohsen U R, Hentschel U (2016); Front Microbiol., 7:1751. doi: 10.3389/fmicb.2016.01751

Shedding light on cell compartmentation in the candidate phylum Poribacteria by high resolution visualisation and transcriptional profiling.

Jahn M T, Markert S M, Ryu T, Ravasi T, Stigloher C, U Hentschel, Moitinho-Silva L (2016); Scientific Reports, 6:35860. doi: 10.1038/srep35860

Population structure and connectivity in the Mediterranean sponge Ircinia fasciculata are affected by mass mortalities and hybridization.

Riesgo A, Pérez-Portela R, Pita L, Blasco G, Erwin P M, López-Legentil S (2016); Heredity, 117:427–439. doi: 10.1038/hdy.2016.41

Grapevine (Vitis vinifera) Crown Galls Host Distinct Microbiota.

Faist H, Keller A, Hentschel U, Deeken R (2016); Appl Environ Microbiol., 82(18):5542-52. doi: 10.1128/AEM.01131-16

Using Nematostella vectensis to Study the Interactions between Genome, Epigenome, and Bacteria in a Changing Environment.

Fraune S, Forêt S, Reitzel A M (2016); Front. Mar. Sci., 3:148. doi: 10.3389/fmars.2016.00148

Williamsia herbipolensis nov., isolated from the phyllosphere of Arabidopsis thaliana.

Kämpfer P, Busse H J, Horn H, Abdelmohsen U R, Hentschel U, Glaeser S P (2016); Int J Syst Evol Microbiol., doi: 10.1099/ijsem.0.001398

Global Sponge Microbiome: Diversity, structure and convergent evolution of symbiont communities across the phylum Porifera.

Thomas T, Moitinho-Silva L, Lurgi M, Björk J R, Easson C, Astudillo C, Olson J B, Erwin P M, López-Legentil S, Luter H, C haves-Fonnegra A, Costa R, Schupp P, Steindler L, Erpenbeck D, Gilbert J, Knight R, Ackerman G, Lopez J V, Taylor M W, Thacker R , Montoya J M, Hentschel U, Webster N (2016); Nat Commun., 7:11870. doi: 10.1038/ncomms11870

Diversity, structure and convergent evolution of the global sponge microbiome.

Thomas T, Moitinho-Silva L, Lurgi M, Björk J R, Easson C, Astudillo-García C, Olson J B, Erwin P M, López-Legentil S, Luter H, Chaves-Fonnegra A, Costa R, Schupp P J, Steindler L, Erpenbeck D, Gilbert J, Knight R, Ackermann G, Victor Lopez J, Taylor M W, Thacker R W, Montoya J M, Hentschel U, Webster N S (2016); Nat Commun., 7:11870. doi: 10.1038/ncomms11870

Response of bacterial colonization in Nematostella vectensis to development, environment and biogeography.

Mortzfeld B M, Urbanski S, Reitzel A M, Künzel S, Technau U, Fraune S (2016); Environ Microbiol., 18(6):1764-81. doi: 10.1111/1462-2920.12926

Hologenome analysis of two marine sponges with different microbiomes.

Ryu T, Seridi L, Moitinho-Silva L, Oates M, Liew Y J, Mavromatis C, Wang X, Haywood A, Lafi F F, Kupresanin M, Sougrat R, Alzahrani M A, Giles E, Ghosheh Y, Schunter C, Baumgarten S, Berumen M L, Gao X, Aranda M, Foret S, Gough J, Voolstra C R, Hentschel U, Ravasi T (2016); BMC Genomics., 17:158. doi: 10.1186/s12864-016-2501-0

Draft genome of the Arabidopsis thaliana phyllosphere bacterium, Williamsia sp. ARP1.

Horn H, Keller A, Hildebrandt U, Kämpfer P, Riederer M, Hentschel U (2016); Stand Genomic Sci., 11:8. doi: 10.1186/s40793-015-0122-x

2015

Draft genome sequences of three chemically rich actinomycetes isolated from Mediterranean sponges.

Horn H, Cheng C, Edrada-Ebel R, Hentschel U, Abdelmohsen U R (2015); Mar Genomics., 24(3):285-7. doi: 10.1016/j.margen.2015.10.003

Inhibitory activities of the marine streptomycete-derived compound SF2446A2 against Chlamydia trachomatis and Schistosoma mansoni.

Reimer A, Blohm A, Quack T, Grevelding C G, Kozjak-Pavlovic V, Rudel T, Hentschel U, Abdelmohsen U R (2015); J Antibiot (Tokyo)., 68(11):674-9. doi: 10.1038/ja.2015.54

Elicitation of secondary metabolism in actinomycetes.

Abdelmohsen U R, Grkovic T, Balasubramanian S, Kamel M S, Quinn R J, Hentschel U (2015); Biotechnol Adv., 33(6Pt1):798-811. doi: 10.1016/j.biotechadv.2015.06.003

Mining Genomes of Three Marine Sponge-Associated Actinobacterial Isolates for Secondary Metabolism.

Horn H, Hentschel U, Abdelmohsen U R (2015); Genome Announc., 3(5). pii:e01106-15. doi: 10.1128/genomeA.01106-15

Biodiversity, Anti-Trypanosomal Activity Screening, and Metabolomic Profiling of Actinomycetes Isolated from Mediterranean Sponges.

Cheng 1, MacIntyre L, Abdelmohsen U R, Horn H, Polymenakou P N, Edrada-Ebel R, Hentschel U (2015); PLoS One., 10(9):e0138528. doi: 10.1371/journal.pone.0138528

Bacteria-bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance

Fraune S, Franzenburg S, Schröder S, Augustin R, Anton-Erxleben F, Bosch TCG. (2015); ISME Journal, 9:1543–1556. doi: 10.1038/ismej.2014.239

Which games are growing bacterial populations playing?

Li XY, Pietschke C, Fraune S, Altrock PM, Bosch TC, Traulsen A (2015); J R Soc Interface., 12(108). doi: 10.1098/rsif.2015.0121

Lifestyle evolution in cyanobacterial symbionts of sponges.

Burgsdorf I, Slaby B M, Handley K M, Haber M, Blom J, Marshall C W, Gilbert J A, Hentschel U, Steindler L (2015); MBio., 6(3):e00391-15. doi: 10.1128/mBio.00391-15

Actinokineospora spheciospongiae sp. nov., isolated from the marine sponge Spheciospongia vagabunda.

Kämpfer P, Glaeser S P, Busse H J, Abdelmohsen U R, Ahmed S, Hentschel U (2015); Int J Syst Evol Microbiol., 65(Pt3):879-84. doi: 10.1099/ijs.0.000031

Antichlamydial sterol from the Red Sea sponge Callyspongia aff. implexa.

Abdelmohsen U R, Cheng C, Reimer A, Kozjak-Pavlovic V, Ibrahim A K, Rudel T, Hentschel U, Edrada-Ebel R, Ahmed S A (2015); Planta Med., 81(5):382-7. doi: 10.1055/s-0035-1545721
.

Symbiotic archaea in marine sponges show stability and host specificity in community structure and ammonia oxidation functionality

Zhang F, Pita Galán L, Erwin P M, Abaid S, López-Legentil S, Russell T H (2015); FEMS Microbiology Ecology, 90(3):699-707. doi: 10.1111/1574-6941.12427

2014

Endophytes are hidden producers of maytansine in Putterlickia roots.

Kusari S, Lamshöft M, Kusari P, Gottfried S, Zühlke S, Louven K, Hentschel U, Kayser O, Spiteller M.(2014); J Nat Prod., 77(12):2577-84. doi: 10.1021/np500219a

How do environmental factors influence life cycles and development? An experimental framework for early-diverging metazoans.

Bosch T C, Adamska M, Augustin R, Domazet-Loso T, Foret S, Fraune S, Funayama N, Grasis J, Hamada M, Hatta M, Hobmayer B, Kawai K, Klimovich A, Manuel M, Shinzato C, Technau U, Yum S, Miller D J(2014); Bioessays., 36(12):1185-94. doi: 10.1002/bies.201400065

GeoChip-based insights into the microbial functional gene repertoire of marine sponges (high microbial abundance, low microbial abundance) and seawater.

Bayer K, Moitinho-Silva L, Brümmer F, Cannistraci C V, Ravasi T, Hentschel U (2014); FEMS Microbiol Ecol., 90(3):832-43. doi: 10.1111/1574-6941.12441

New antibacterial xanthone from the marine sponge-derived Micrococcus sp. EG45.

Eltamany E E, Abdelmohsen U R, Ibrahim A K, Hassanean H A, Hentschel U, Ahmed S A(2014); Bioorg Med Chem Lett., 24(21):4939-42. doi: 10.1016/j.bmcl.2014.09.040

Two new antioxidant actinosporin analogues from the calcium alginate beads culture of sponge-associated Actinokineospora sp. strain EG49.

Grkovic T, Abdelmohsen U R, Othman E M, Stopper H, Edrada-Ebel R, Hentschel U, Quinn R J (2014); Bioorg Med Chem Lett.,24(21):5089-92. doi: 10.1016/j.bmcl.2014.08.068

Species-specific viromes in the ancestral holobiont Hydra.

Grasis J A, Lachnit T, Anton-Erxleben F, Lim Y W, Schmieder R, Fraune S, Franzenburg S, Insua S, Machado G, Haynes M, Little M, Kimble R, Rosenstiel P, Rohwer F L, Bosch T C (2014); PLoS One., 9(10):e109952. doi: 10.1371/journal.pone.0109952

Revealing microbial functional
activities in the Red Sea sponge Stylissa carteri by metatranscriptomics.

Moitinho-Silva L, Seridi L, Ryu T, Voolstra C R, Ravasi T, Hentschel U (2014); Environ Microbiol, 16(12):3683–3698.  
doi: 10.1111/1462-2920.12533

An environmental
 bacterial taxon with a large and distinct metabolic repertoire.

Wilson M C, Mori T, Rückert C, Uria A R, Helf M J, Takada K, Gernert C, Steffens U A, Heycke N, 
Schmitt S, Rinke C, Helfrich E J, Brachmann A O, Gurgui C, Wakimoto T, Kracht M, Crüsemann M,
 Hentschel U, Abe I, Matsunaga S, Kalinowski J, Takeyama H, Piel J (2014); Nature, 506:58-62. doi: 10.1038/nature12959

2013

Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial
symbionts of marine sponges.

Kamke J, Sczyrba A, Ivanova N, Schwientek P, Rinke C, Mavromatis K, Woyke T, Hentschel U
 (2013); ISME J, 7(12):2287-2300. doi: 10.1038/ismej.2013.111

Bacterial colonization of Hydra hatchlings follows a robust temporal pattern.

Franzenburg S, Fraune S, Altrock P M, Künzel S, Baines J F, Traulsen A, Bosch T C G (2013); ISME J., 7(4):781-90. doi: 10.1038/ismej.2012.156

Distinct antimicrobial peptide expression determines host species-specific bacterial associations

Franzenburg S, Walter J, Künzel S, Wang J, Baines J F, Bosch T C G, Fraune S (2013); Proc Natl Acad Sci USA, 110(39):E3730-8. doi: 10.1073/pnas.1304960110

Till death does us apart: Stable sponge-bacteria associations under thermal and food shortage stresses

Pita Galán L, Erwin P M, Turon X, López-Legentil S (2013); PLoS One, 8(11):e80307. doi: 10.1371/journal.pone.0080307

Host rules: spatial stability of bacterial communities associated with marine sponges (Ircinia spp) in the Western Mediterranean Sea

Pita Galán L, Turon X, López-Legentil S, Erwin P M (2013); FEMS Microbiology Ecology, 86(2):286-276. doi: 10.1111/1574-6941.12159

Biogeography and host fidelity of bacterial communities in Ircinia spp from the Bahamas

Pita Galán L, López-Legentil S, Erwin P M (2013); Microb Ecol., 66:437-447. doi: 10.1007/s00248-013-0215-2

Animals in a bacterial world, a new imperative for the life sciences.

McFall-Ngai M, Hadfield M, Bosch T C G, Carey H, Domazet-Loso T, Douglas A, Dubilier N, Eberl G, Fukami T, Gilbert S, Hentschel U, King N, Kjelleberg S, Knoll A, Kremer N, Mazmanian S, Metcalf J, Nealson K, Pierce N, Rawls J, Reid A, Ruby E, Rumpho M, Sanders J, Tautz D, Wernegreen J (2013); Proc Natl Acad Sci USA, 110(9):3229-36. doi: 10.1073/pnas.1218525110

2012

Assessing the complex sponge microbiota – core,
variable, and species-specific bacterial communities in marine sponges.

Schmitt S, Tsai P, Bell J, Fromont F, Ilan M, Lindquist N L, Perez T, Rodrigo A, Schupp P J, Vacelet 
J, Webster N, Hentschel U, Taylor M W (2012); ISME J, 6(3): 564-57. doi: 10.1038/ismej.2011.116

Genomic insights into the marine sponge microbiome.

Hentschel U, Piel J, Degnan S M, Taylor M W (2012);
 Nat Rev Microbiol., 10(9): 641-654. doi: 10.1038/nrmicro2839

Hydra meiosis reveals unexpected conservation of structural synaptonemal complex proteins across metazoans.

Fraune J, Alsheimer M, Volff JN, Busch K, Fraune S, Bosch T C G, Benavente R (2012); Proc. Natl. Acad. Sci. USA, 109:16588-16593. doi: 10.1073/pnas.1206875109

MyD88-deficient Hydra reveal an ancient function of TLR signaling in sensing bacterial colonizers.

Franzenburg S, Fraune S, Künzel S, Baines J F, Domazet-Loso T, Bosch T C G (2012); Proc Natl Acad Sci USA, 109(47):19374-9. doi: 10.1073/pnas.1213110109

MyD88 deficient Hydra reveal an ancient function of TLR-signaling in sensing bacterial colonizers.

Franzenburg S, Fraune S, Künzel S, Baines J F, Domazet-Loso T, Bosch T C (2012); Proc Natl Acad Sci U S A., 109(47):19374-9. doi: 10.1073/pnas.1213110109

Stability of sponge-associated bacteria over large seasonal shifts in temperature and irradiance

Erwin P M, Pita Galán L, López-Legentil S, Turon X (2012); Appl Environ Microbiol., 78(20):7358-7368. doi: 10.1128/AEM.02035-12

Where simplicity meets complexity: hydra, a model for host-microbe interactions.

Augustin R, Fraune S, Franzenburg S, Bosch T C (2012); Adv Exp Med Biol., 710:71-81. doi: 10.1007/978-1-4419-5638-5_8

2011

Time and space:genetic structure of the cohorts of the common sea urchin Paracentrotus lividus in Western Mediterranean

Calderón I, Pita Galán L, Brusciotti S, Palacín C, Turon X (2011); Mar Biol, 159:187-197. doi: 10.1007/s00227-011-1799-z

Embryo protection in contemporary immunology: Why bacteria matter.

Fraune S, Augustin R, Bosch T C (2011); Commun Integr Biol., 4(4):369-72. doi: 10.4161/cib.4.4.15159

Single
-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated
with marine sponges.

Siegl A, Kamke J, Hochmuth T, Piel J, Richter M, Liang C, Dandekar T, Hentschel U (2011); ISME J, 5(1):61-70. doi: 10.1038/ismej.2010.95

2010

In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides

Fraune S, Augustin R, Anton-Erxleben F, Wittlieb J, Gelhaus C, Klimovich VB, Samoilovich MP, Bosch TCG (2010); Proc. Natl. Acad. Sci., 107(42):18067-18072. doi: 10.1073/pnas.1008573107

Why bacteria matter in animal development and evolution.

Fraune S,Bosch T C G (2010); Bioessays, 32(7):571-80. doi: 10.1002/bies.200900192

The dynamic genome of Hydra.

Chapman J A, Kirkness E F, Simakov O, Hampson S E, Mitros T, Weinmaier T, Rattei T, Balasubramanian P G, Borman J, Busam D, Disbennett K, Pfannkoch C, Sumin N, Sutton G G, Viswanathan L D, Walenz B, Goodstein D M, Hellsten U, Kawashima T, Prochnik S E, Putnam N H, Shu S, Blumberg B, Dana C E, Gee L, Kibler D F, Law L, Lindgens D, Martinez D E, Peng J, Wigge P A, Bertulat B, Guder C, Nakamura Y, Ozbek S, Watanabe H, Khalturin K, Hemmrich G, Franke A, Augustin R, Fraune S, Hayakawa E, Hayakawa S, Hirose M, Hwang J S, Ikeo K, Nishimiya-Fujisawa C, Ogura A, Takahashi T, Steinmetz P R, Zhang X, Aufschnaiter R, Eder M K, Gorny A K, Salvenmoser W, Heimberg A M, Wheeler B M, Peterson K J, Böttger A, Tischler P, Wolf A, Gojobori T, Remington K A, Strausberg R L, Venter J C, Technau U, Hobmayer B, Bosch T C G, Holstein T W, Fujisawa T, Bode H R, David C N, Rokhsar D S, Steele R E (2010); Nature, 464:592-6. doi: 10.1038/nature08830

How Hydra senses and destroys microbes.

Augustin R , Fraune S, Bosch T C (2010); Semin Immunol., 22(1):54-8. doi: 10.1016/j.smim.2009.11.002

2009

Is activated hemocyanin instead of phenoloxidase involved in immune response in woodlice?

Jaenicke E, Fraune S, May S, Irmak P, Augustin R, Meesters C, Decker H, Zimmer M (2009); Dev Comp Immunol., 33(10):1055-63. doi: 10.1016/j.dci.2009.05.005

Disturbing epithelial homeostasis in the metazoan Hydra leads to drastic changes in associated microbiota.

Fraune S, Abe Y, Bosch T C G (2009); Environ. Microbiol., 11(9):2361-2369. doi: 10.1111/j.1462-2920.2009.01963.x

More than just orphans: are taxonomically-restricted genes important in evolution?

Khalturin K, Hemmrich G, Fraune S, Augustin R, Bosch T C (2009); Trends Genet., 25(9):404-13. doi: 10.1016/j.tig.2009.07.006

Uncovering the evolutionary history of innate immunity: the simple metazoan Hydra uses epithelial cells for host defence.

Bosch T C, Augustin R, Anton-Erxleben F, Fraune S, Hemmrich G, Zill H, Rosenstiel P, Jacobs G, Schreiber S, Leippe M, Stanisak M, Grötzinger J, Jung S, Podschun R, Bartels J, Harder J, Schröder J M (2009); Dev Comp Immunol., 33(4):559-69. doi: 10.1016/j.dci.2008.10.004

Plasticity of epithelial cell shape in response to upstream signals: a whole-organism study using transgenic Hydra.

Anton-Erxleben F, Thomas A, Wittlieb J, Fraune S, Bosch TC (2009); Zoology (Jena), 112(3):185-94. doi: 10.1016/j.zool.2008.09.002

2008

Molecular microbial diversity
survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial
symbionts.

Schmitt S, Angermeier H, Schiller R, Lindquist N, Hentschel U (2008); Appl Environ Microbiol, 74:7694-7708. doi: 10.1128/AEM.00878-08

Physiology, phylogeny and in-situ evidence for bacterial
and archaeal nitrifiers in the marine sponge Aplysina aerophoba.

Bayer K, Schmitt S, Hentschel U (2008); Environ Microbiol, 10(11):2942-
2955. doi: 10.1111/j.1462-2920.2008.01582.x

2007

Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra.

Fraune S, Bosch TCG (2007); Proc Natl Acad Sci USA, 104(32):13146-51. doi: 10.1073/pnas.0703375104

2004

Discovery of a novel candidate phylum ‘Poribacteria’
in marine sponges.

Fieseler L, Horn M, Wagner M, Hentschel U (2004); Appl Environ Microbiol, 70(6):3724-3732. doi: 10.1128/AEM.70.6.3724-3732.2004