Towards understanding an ultimately simple metaorganism: impact of symbiotic microbes and algae on developmental processes of Hydra

Inter-species interactions in the freshwater polyp Hydra between symbiotic algae and host cells had been the subject of research since decades since they not only provide insights into the basic “tool kit” necessary to establish symbiotic interactions, but are also of relevance in understanding the resulting evolutionary selection processes. A long term persistence of symbiotic associations is prevalent not only in two-party interactions of Hydra and symbiotic algae, but also in more complex systems including stable associated bacteria. Studying symbiotic inter-species interactions in Hydra, therefore, may be a paradigmatic example of a complex symbiotic community that influences the host´s health and development. Starting from one of “the” classical model systems in developmental biology, we used Hydra in the last few years to explore host-microbe interactions. Our findings reveal that epithelia and components of the innate immune system play an active role in selecting the inhabitant microbiota via a complex genetic network. The work has contributed to a paradigm shift in evolutionary immunology:

Components of the innate immune system with its host-specific antimicrobial peptides appear to have evolved in early branching metazoans because of the need to control the resident beneficial microbes rather than because of invasive pathogens. Yet in spite of all these insights in an ultimately simple metaorganism we have still not been able to coherently integrate the accumulated abundance of information into a truly mechanistic understanding of host-microbe interactions. To understand common principles of symbiogenesis and their links to metaorganism evolution, we examine the impact of symbiotic microbes and algae on developmental processes in Hydra.

Elucidating these issues will not only contribute to our understanding of the genetic basis of microbial speciation and adaptation within eukaryotic hosts but will also provide conceptual insights into the impact of beneficial microbes on the host life history and the complexity of host-microbe interactions in general.


Jay Bathia

PhD Candidate
Kiel University Zoological Institute

Dr. Peter Deines

Postdoctoral Researcher, Associated Junior Researcher
Kiel University Zoological Institute

Risa Taira

PhD Candidate, Alumni
Kiel University Zoological Institute

Jinru He

PhD Candidate
Kiel University Zoological Institute



Back to the Basics: Cnidarians Start to Fire.

Bosch T C, Klimovich A, Domazet-Lošo T, Gründer S, Holstein T W, Jékely G, Miller D J, Murillo-Rincon A P, Rentzsch F, Richards G S, Schröder K, Technau U, Yuste R (2017); Trends Neurosci., 40(2):92-105. doi: 10.1016/j.tins.2016.11.005


FRT – FONDATION RENE TOURAINE: An International Foundation For Dermatology.

Bosch T C, Zengler K, Naik S, Biedermann T, Kong H H, Loser K, Brüggeman H, Calleawert C, Lambert J, Van de Wiele T (2016); Exp Dermatol., 25(11):917-932. doi: 10.1111/exd.13160

Impact of explantation techniques on the microbiota of the marine sponge Ecionemia alata.

Meyer K M, Deines P, Schupp P J, Taylor M W (2016); Journal of Experimental Marine Biology and Ecology, 484:11–15. doi: 10.1016/j.jembe.2016.08.003

The Origin of Mucosal Immunity: Lessons from the Holobiont Hydra.

Schröder K, Bosch T C (2016); MBio., 7(6):e01184-16. doi: 10.1128/mBio.01184-16

Transitioning from Microbiome Composition to Microbial Community Interactions: The Potential of the Metaorganism Hydra as an Experimental Model.

Deines P, Bosch T C G (2016); Front. Microbiol., 7:1610. doi: 10.3389/fmicb.2016.01610

Understanding why we age and how: Evolutionary biology meets different model organisms and multi-level omics.

Gilson E, Bosch T C G (2016); Meeting report on “Comparative Biology of Aging”, Roscoff, October 12-16, 2015. BioEssays, 38(6):494-97. doi: 10.1002/bies.201600049

In four shallow and mesophotic tropical reef sponges from Guam the microbial community largely depends on host identity.

Steinert G, Taylor M W, Deines P, Simister R L, de Voogd N J, Hoggard M, Schupp P J (2016); PeerJ., 4:e1936. doi: 10.7717/peerj.1936

Getting the Hologenome Concept Right: An Eco-Evolutionary Framework for Hosts and Their Microbiomes.

Theis K R, Dheilly N M, Klassen J L, Brucker R M, Baines J F, Bosch T C, Cryan J F, Gilbert S F, Goodnight C J, Lloyd E A, Sapp J, Vandenkoornhuyse P, Zilber-Rosenberg I, Rosenberg E, Bordenstein S R (2016); mSystems., 1(2).pii:e00028-16. doi: 10.1128/mSystems.00028-16

The Holobiont Imperative.

Bosch T C G and D Miller (2016); Springer New York, ISBN: 978-3-7091-1894-8


Life cycle reversal in Aurelia sp. 1 (Cnidaria, Scyphozoa).

He J, Zheng L, Zhang W, Lin Y (2015); PLoS One, 10(12):e0145314. doi: 10.1371/journal.pone.0145314

Revisiting the age, evolutionary history and species level diversity of the genus Hydra (Cnidaria: Hydrozoa).

Schwentner M, Bosch T C (2015); Mol Phylogenet Evol., 91:41-55. doi: 10.1016/j.ympev.2015.05.013

Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents.

Gilbert S F, Bosch T C, Ledón-Rettig C (2015); Nat Rev Genet., 16(10):611-622. doi: 10.1038/nrg3982

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

Microbial community structure in the gut of the New Zealand insect Auckland tree weta (Hemideina thoracica).

Waite D W, Dsouza M, Biswas K, Ward D F, Deines P, Taylor M W (2015); Arch Microbiol., 197(4):603-12. doi: 10.1007/s00203-015-1094-3

Morphology and molecular analyses of a new Clytia species (Cnidaria: Hydrozoa: Campanulariidae) from the East China Sea.

He J, Zheng L, Zhang W, Lin Y, Cao W (2015); Journal of the Marine Biological Association of the United Kingdom, 95(2):289-300. doi: 10.1017/S0025315414000836

Microbial ecology in Hydra: Why viruses matter.

Bosch T C G, Grasis J A, Lachnit T (2015); J Microbiol, 53(3):193-200. doi: 10.1007/s12275-015-4695-2

Microbial ecology in Hydra: Why viruses matter.

Bosch T C, Grasis J, Lachnit T (2015); The Journal of Microbiology, 53(3):193-200. doi: 10.1007/s12275-015-4695-2

Hydra and the evolution of stem cells.

Klimovich A, Böhm A M, Bosch T C G (2015); „Stem cell biology and regenerative medicine” River Publishers, 113-136. ISBN: 9788793237070


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

Methodological approaches for studying the microbial ecology of drinking water distribution systems.

Douterelo I, Boxall J B, Deines P, Sekar R, Fish KE , Biggs C A (2014); Water Res., 65:134-56. doi: 10.1016/j.watres.2014.07.008

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

Rethinking the role of immunity: lessons from Hydra

Bosch T C G (2014); Trends Immunol., 35(10):495-502. doi: 10.1016/j.it.2014.07.008

Naturally occurring tumors in the basal metazoan Hydra.

Domazet-Lošo T, Klimovich A, Anokhin B, Anton-Erxleben F, Hamm M, Lange C, Bosch T C G (2014); Nat Communications, 5:4222. doi: 10.1038/ncomms5222

16S rRNA is a better choice than COI for DNA barcoding hydrozoans in the coastal waters of China.

Zheng L, He J, Lin Y, Cao W, Zhang W (2014); Acta Oceanologica Sinica, 33(4):1-22. doi: 10.1007/s13131-014-0415-8

Regulation of polyp-to-jellyfish transition in Aurelia aurita.

Fuchs B, Wang W, Graspeuntner S, Li Y, Insua S, Herbst E M, Dirksen P, Bohm A M, Hemmrich G, Sommer F, Domazet-Loso T, Klostermeier U C, Anton-Erxleben F, Rosenstiel P, Bosch T C, Khalturin K (2014); Curr Biol, 24(3):263-273. doi: 10.1016/j.cub.2013.12.003


Detection of a new Clytia species (Cnidaria: Hydrozoa: Campanulariidae) with DNA barcoding and life cycle analyses.

Zhou K, Zheng L, He J, Lin Y, Cao W, Zhang W (2013); Journal of the Marine Biological Association of the United Kingdom, 93(8):2075-2088. doi: 10.1017/S0025315413000969

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

Quantifying the impact of storage procedures for faecal bacteriotherapy in the critically endangered New Zealand parrot, the kakapo (Strigops habroptilus).

Waite D W, Deines P, Taylor M W (2013); Zoo Biol., 32(6):620-5. doi: 10.1002/zoo.21098

Temporal molecular and isotopic analysis of active bacterial communities in two New Zealand sponges.

Simister R, Taylor M W, Rogers K M, Schupp P J, Deines P (2013); FEMS Microbiol Ecol., 85(1):195-205. doi: 10.1111/1574-6941.12109

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

‘Sponge-specific’ bacteria are widespread (but rare) in diverse marine environments.

Taylor M W, Tsai P, Simister R L, Deines P, Botte E, Ericson G, Schmitt S, Webster N S (2013); ISME J., 7(2):438-43. doi: 10.1038/ismej.2012.111


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

FoxO is a critical regulator of stem cell maintenance and immortality in Hydra.

Boehm A M, Hemmrich G, Khalturin K, Puchert M, Anton-Erxleben F, Wittlieb J, Klostermeier U C, Rosenstiel P, Oberg H H, Bosch T C G (2012); Proc Natl Acad Sci USA, 109(48):19697-702. doi: 10.1073/pnas.1209714109

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

Blood system formation in the urochordate Ciona intestinalis requires the variable receptor vCRL1.

Sommer F, Awazu S, Anton-Erxleben F, Jiang D, Klimovich A V, Klimovich B V, Samoilovich M P, Satou Y, Krüss M, Gelhaus C, Kürn U, Bosch T C, Khalturin K (2012); Mol Biol Evol., 29(10): 3081-3093. doi: 10.1093/molbev/mss120

Ultrastructural and molecular characterization of a bacterial symbiosis in the ecologically important scale insect family Coelostomidiidae.

Dhami M K, Turner A P, Deines P, Beggs J R, Taylor M W (2012); FEMS Microbiol Ecol., 81(3):537-46. doi: 10.1111/j.1574-6941.2012.01378.x

Bacterial water quality and network hydraulic characteristics: a field study of a small, looped water distribution system using culture-independent molecular methods.

Sekar R, Deines P, Machell J, Osborn A M, Biggs C A, Boxall J B (2012); J Appl Microbiol., 112(6):1220-34. doi: 10.1111/j.1365-2672.2012.05286.x

Quantitative genetics of immunity and life history under different photoperiods.

Hammerschmidt K, Deines P, Wilson A J, Rolff J (2012); Heredity (Edinb)., 108(5):569-76. doi: 10.1038/hdy.2011.125

Gut microbiome of the critically endangered New Zealand parrot, the kakapo (Strigops habroptilus).

Waite D W, Deines P, Taylor M W (2012); PLoS One., 7(4):e35803. doi: 10.1371/journal.pone.0035803

In vitro transition of Schistocephalus solidus (Cestoda) from coracidium to procercoid and from procercoid to plerocercoid.

Jakobsen P J, Scharsack J P, Hammerschmidt K, Deines P, Kalbe M, Milinski M (2012); Exp Parasitol., 130(3):267-73. doi: 10.1016/j.exppara.2011.09.009

Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms.

Simister R L, Deines P, Botté E S, Webster N S, Taylor M W (2012); Environ Microbiol., 14(2):517-24. doi: 10.1111/j.1462-2920.2011.02664.x

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


The potential of methanotrophic bacteria to compensate for food quantity or food quality limitations in Daphnia.

Deines P, Fink P (2011); Aquat Microb Ecol, 65:197-206. doi: 10.3354/ame01542

Chloroflexi bacteria are more diverse, abundant, and similar in high than in low microbial abundance sponges.

Schmitt S, Deines P, Behnam F, Wagner M, Taylor M W (2011); FEMS Microbiol Ecol., 78(3):497-510. doi: 10.1111/j.1574-6941.2011.01179.x

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

Effect of temperature on the substrate utilization profiles of microbial communities in different sewer sediments.

Biggs C A, Olaleye O I, Jeanmeure L F, Deines P, Jensen H S, Tait S J, Wright P C (2011); Environ Technol., 32(1-2):133-44. doi: 10.1080/09593330.2010.490852


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

MUWS (Microbiology in Urban Water Systems) – an interdisciplinary approach to study microbial communities in urban water systems.

Deines P, Sekar P, Jensen H, Tai, S, Boxall J, Osborn A and Biggs C (2010); Drinking Water Engineering and Science, 3(2):91-99. doi: 10.5194/dwes-3-91-2010

A new coupon design for simultaneous analysis of in situ microbial biofilm formation and community structure in drinking water distribution systems.

Deines P, Sekar R, Husband P S, Boxall J B, Osborn A M, Biggs C A (2010); Appl Microbiol Biotechnol., 87(2):749-56. doi: 10.1007/s00253-010-2510-x

Development of immunoreagents for diagnostics of CagA-positive Helicobacter pylori infections.

Klimovich A V, Samoylovich M P, Gryazeva I V, Terekhina L A, Suvorov A N, Klimovich V B (2010); Helicobacter. 15(3):193-200. doi: 10.1111/j.1523-5378.2010.00754.x

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


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

Himasthla elongata: effect of infection on expression of the LUSTR-like receptor mRNA in common periwinkle haemocytes.

Gorbushin A M, Klimovich A V, Iakovleva N V (2009); Exp Parasitol., 123(1):24-30. doi: 10.1016/j.exppara.2009.05.004

Unravelling complexities in benthic food webs using a dual stable isotope (hydrogen and carbon) approach.

Deines P, Wooller M J, Grey J (2009); Freshwater Biology, 54(11):2243-2251. doi: 10.1111/j.1365-2427.2009.02259.x

Toxicity of violacein-producing bacteria fed to bacterivorous freshwater plankton.

Deines P, Matz C, Jürgens K (2009); Limnol. Oceanogr., 54(4):1343–1352. ISSN: 0024-3590

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


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

Methane-derived carbon flows through methane-oxidizing bacteria to higher trophic levels in aquatic systems.

Deines P, Bodelier P L, Eller G (2007); Environ Microbiol., 9(5):1126-34. doi: 10.1111/j.1462-2920.2006.01235.x

Possible sources of methane-derived carbon for chironomid larvae.

Eller G, Deines P, Krüger M (2007); AME, 46:3 doi: 10.3354/ame046283

Linking larval chironomids to methane:seasonal variation of the microbial methane cycle and chironomid δ13C.

Deines P, Grey J, Richnow H H, Eller G (2007); Aquatic Microbial Ecology, 46:273-282. doi: 10.3354/ame046273

Allorecognition in urochordates: identification of a highly variable complement receptor-like protein expressed in follicle cells of Ciona.

Kurn U, Sommer F, Hemmrich G, Bosch T C, Khalturin K (2007); Dev Comp Immunol., 31(4):360-371. doi: 10.1016/j.dci.2006.06.008


In the urochordate Ciona intestinalis zona pellucida domain proteins vary among individuals.

Kurn U, Sommer F, Bosch T C, Khalturin K (2006); Developmental and comparative immunology, 31(12): 1242-1254. doi: 10.1016/j.dci.2007.03.011

Alternate unstable states: Convergent paths of succession in hydrocarbon-seep tubeworm-associated communities.

Cordes E E B, Bergquist D C, Predmore B L, Jones C, Deines P, Telesnickia G, Fisher C R (2006); Journal of Experimental Marine Biology and Ecology, 339(2):159–176. doi: 10.1016/j.jembe.2006.07.017

Site-specific methane production and subsequent midge mediation within Esthwaite Water, UK.

Deines P, Grey J (2006); Archiv für Hydrobiologie, 167(1-4):317-334. doi: 10.1127/0003-9136/2006/0167-0317

Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis.

Wittlieb J, Khalturin K, Lohmann J, Anton-Erxleben F, Bosch T C G (2006); Proc. Natl. Acad. Sci. USA, 103(16):6208-6211. doi: 10.1073/pnas.0510163103


Methane cycling in lake sediments and its influence on chironomid larval delta13C.

Eller G, Deines P, Grey J, Richnow H H, Krüger M (2005); FEMS Microbiol Ecol., 54(3):339-50. doi: 10.1016/j.femsec.2005.04.006

Differential assimilation of methanotrophic and chemoautotrophic bacteria by lake chironomid larvae

Grey J, Deines P (2005); AME, 40(1):61-66. doi: 10.3354/ame040061


Impact of violacein-producing bacteria on survival and feeding of bacterivorous nanoflagellates.

Matz C, Deines P, Boenigk J, Arndt H, Eberl L, Kjelleberg S, Jürgens K (2004); Appl Environ Microbiol., 70(3):1593-9. doi: 10.1128/AEM.70.3.1593-1599.2004


Phenotypic variation in Pseudomonas sp. CM10 determines microcolony formation and survival under protozoan grazing

Matz C, Deines P, Jürgens K (2002); FEMS Microbiol Ecol., 39(1):57-65. doi: 10.1111/j.1574-6941.2002.tb00906.x