B2
Recognition and Communication

Microbiota-host interactions at the base of the metazoan tree

The project continues to address the establishment and functional consequences of the microbiota in the two basal metazoan animals, the Scyphozoan jellyfish Aurelia aurita (Cnidaria) (B2.1, PI Schmitz-Streit) and the comb jelly Mnemiopsis leidyi (Ctenophora) (B2.2, PI Reusch) in a highly comparative approach.

Analysis of the associated microbial community composition of these two metazoan animals during the first funding phase, led to the identification of 16 bacterial key species responsible for community differences. Out of 16 operational taxonomic units (OTUs), eleven were present in both communities, in different ratios, with four restricted to M. leidyi and one to A. aurita. Moreover, 25 representatives of these indicator OTUs are already isolated, which can be used for recolonization experiments planned in the second phase.
We further demonstrated that (i) life stage-specific bacterial community patterns of A. aurita undergo significant restructuring during metamorphosis, and obtained first experimental evidence that the associated microbes are crucial for reproductive output of the host. (ii) A. aurita-derived Quorum Quenching (QQ) activities are enhanced upon challenging with pathogens and interfere with bacterial Quorum Sensing; in case of M. leidyi screening EST libraries demonstrated even higher numbers of host-derived QQ activities. (iii) A two-generation (F2) evolution experiment using two different base populations of M. leidyi demonstrated rapid adaptation of growth and reproduction to contrasting salinity levels, which coincided with significant changes in the microbiota, suggesting an important role of the microbiota for rapid responses of M. leidyi to environmental change. Under low salinity challenge, we identified ten indicator OTUs, several of which have been isolated during the first funding phase and will serve as critical resource during the second phase, when evolution experiments are aimed to assess the functional role of microbes in the invasion process.

Based on this work, the following key questions will be addressed in the second funding phase to elucidate the functional consequences of the microbiota in the two basal metazoan animals:

(i) What is the basis of the observed microbial contribution to A. aurita reproduction? The underlying molecular mechanism will be illuminated with re-colonization experiments of germ-free animals combined with metatranscriptomic and biochemical approaches.

(ii) What is the functionality of QQ activities between microbes for establishing the associated microbiota? Functional assays will be performed using simplified and genetically engineered microbial communities (Mock community) for both hosts to elucidate the importance of the identified QQ open reading frames (ORFs) in respect to a healthy metaorganism.

(iii) Are there conserved host-derived QQ patterns in different metaorganisms (lower metazoan)? This will be addressed by a combination of homology and domain based comparative genome and gene expression pattern analyses.

(iv) What is the function of the associated microbiota for M. leidyi host fitness? Targeted experiments will address the fitness effects of germ-free animals versus animals reconstituted with Mock communities of varying degree of simplification.

(v) What is the importance of microbiota for rapid adaptation during the invasion process of M. leidyi? Using evolution experiments under low salinity conditions versus controls, the role of microbiota for adaptation of the M. leidyi metaorganism will be assessed. By altering the co-evolved microbiota at the end of the selection phase, we can directly address how the associated microbiota influences major fitness traits during invasion.

The overarching questions on the establishment and functional consequences of microbiota will be addressed in a highly comparative way for both hosts combining the complementary expertise of the two PIs in different biological fields. Elucidating these questions will not only contribute to the understanding of host interactions with microbial communities, but also aims to provide conceptual insights into the complexity of host-microbe interactions in general. The identification of underlying principles in basal metazoan-host interactions is imperative to under-stand how metazoan life emerged in a “soup of microbes” in the ocean.

B2
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B2.1: The role of microbiota for A. aurita reproduction and functionality of QQ activities

B2.2: The role of associated microbiota for fitness and invasion success in the comb jelly M. leidyi

B2
Related Publications

Related Publications

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2023
B2

Four novel Caudoviricetes bacteriophages isolated from Baltic Sea water infect colonizers of Aurelia aurita

Stante M, Weiland-Bräuer N, Repnik U, Werner A, Bramkamp M, Chibani CM, Schmitz RA (2023) Four novel Caudoviricetes bacteriophages isolated from Baltic Sea water infect colonizers of Aurelia aurita. Viruses. 2023; 15(7):1525. doi: 10.3390/v1507152
2023
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B2
B4

Comparative genomics of novel Bacteroides acidifaciens isolates reveals candidates for adaptation to host subspecies in house mice

Hanna Fokt, Shauni Doms, Malte C. Rühlemann, Maxime Godfroid, Ruth A. Schmitz, Britt M. Hermes, John F. Baines (2023) Comparative genomics of novel Bacteroides acidifaciens isolates reveals candidates for adaptation to host subspecies in house mice BioRxiv

 

2023
B2

Microbial community changes correlate with impaired host fitness of Aurelia aurita after environmental challenge

Pinnow N, Chibani CM, Güllert S, Weiland-Bräuer N (2023) Microbial community changes correlate with impaired host fitness of Aurelia aurita after environmental challenge. anim microbiome 5, 45 (2023). doi: 10.1186/s42523-023-00266-4

2023
B2

Antimicrobial peptides originating from expression libraries of Aurelia aurita and Mnemiopsis leidyi prevent biofilm formation of opportunistic pathogens

Ladewig L, Gloy L, Langfeldt D, Pinnow N, Weiland-Bräuer N, Schmitz RA (2023) Antimicrobial peptides originating from expression libraries of Aurelia aurita and Mnemiopsis leidyi prevent biofilm formation of opportunistic pathogens. Microorganisms, 11(9), 2184. doi: 10.3390/microorganisms11092184

2023
B2

First insights into the Aurelia aurita transcriptome response upon manipulation of its microbiome

Weiland-Bräuer N, Koutsouveli V, Langfeldt D, Schmitz RA (2023) First insights into the Aurelia aurita transcriptome response upon manipulation of its microbiome. Front. Microbiol. 14:1183627. doi: 10.3389/fmicb.2023.1183627

2023
B2

The Life Cycle of Aurelia aurita Depends on the Presence of a Microbiome in Polyps Prior to Onset of Strobilation

Jensen N, Weiland-Bräuer N, Joel S, Chibani CM, Schmitz RA (2023)  The Life Cycle of Aurelia aurita Depends on the Presence of a Microbiome in Polyps Prior to Onset of Strobilation. Microbiology Spectrum, 11(4), e00262-23. doi: 10.1128/spectrum.00262-23

2023
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Closely related Bacteroides of the murine intestinal microbiota affect each other’s growth positively or negatively

Hanna Fokt, Gabija Sakalyte, Rahul Unni, Mohammad Abukhalaf, Liam Cassidy, Georgios Marinos, Maxime Godfroid, Birhanu M Kinfu, Ruth A Schmitz, Christoph Kaleta, Andreas Tholey, John F Baines, Tal Dagan, Daniel Unterweger (2023) BioRxiv
2021
B2

Invasion genomics uncover contrasting scenarios of genetic diversity in a widespread marine invader.

Jaspers C, Ehrlich M, Pujolar JM, Künzel S, Bayer T, Limborg MT, Lombard F, Browne WE, Stefanova K, Reusch TBH (2021):  PNAS. 118(51)e2116211118. doi: 10.1073/pnas.2116211118

2020
B2

The native microbiome is crucial for offspring generation and fitness of Aurelia aurita

Weiland-Bräuer N, Pinnow N, Langfeldt D, Roik A, Güllert S, Chibani CM, Reusch TBH, Schmitz RA (2020) mBio. 11(6) e02336-20. doi: 10.1128/mBio.02336-20

2020
B2

B-vitamin nutrition in the pea aphid-Buchnera symbiosis

Blow F, Bueno E, Clark N, Zhu TD, Chung SH, Güllert S, Schmitz RA, Douglas AE (2020) Journal of Insect Physiology. 126:104092. doi: 10.1016/j.jinsphys.2020.104092

2020
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Z2

Cultivable microbiota associated with Aurelia aurita and Mnemiopsis leidyi

Weiland-Bräuer N, Prasse D, Brauer A, Jaspers C, Reusch TBH, Schmitz RA (2020) MicrobiologyOpen. 9(9):e1094 doi: 10.1002/mbo3.1094  

2020
A2
B2

Differences in the microbiota of native and non-indigenous gelatinous zooplankton organisms in a low saline environment

Jaspers C, Weiland-Bräuer N, Rühlemann MC, Baines JF, Schmitz RA, Reusch TBH (2020) Sci Total Environ. 734:139471. doi: 10.1016/j.scitotenv.2020.139471

2019
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Advancing our functional understanding of host–microbiota interactions: a need for new types of studies

He J, Lange J, Marinos G, Bathia J, Harris D, Soluch R, Vaibhvi V, Deines P, Hassani MA, Wagner K-S, Zapien‐Campos R, Jaspers C, Sommer F (2019) BioEssays, 1900211 (1-5). doi: 10.1002/bies.201900211

 

2019
B2
INF
Z3

Host-microbe interactions in the chemosynthetic Riftia pachyptila symbiosis

Hinzke T, Kleiner M, Breusing C, Felbeck H, Häsler R, Sievert SM, Schlüter R, Rosenstiel P, Reusch TBH, Schweder T, Markert S (2019) mBio 10:6, e02243-19. doi: 10.1128/mBio.02243-19

2019
B2

Microbiota differences of the comb jelly Mnemiopsis leidyi in native and invasive sub-populations

Jaspers C, Weiland-Bräuer N, Fischer M, Künzel S, Schmitz RA, Reusch TBH (2019) Front. Mar. Sci. 6: 635. doi: 10.3389/fmars.2019.00635

2019
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Comparative analysis of amplicon and metagenomic sequencing methods reveals key features in the evolution of animal metaorganisms

Rausch P, Rühlemann M, Hermes BM, Doms S, Dagan T, Dierking K, Domin H, Fraune S, von Frieling J, Hentschel U, Heinsen F-A, Höppner M, Jahn MT, Jaspers C, Kissoyan KAB, Langfeldt D, Rehman A, Reusch TBH, Roeder T, Schmitz RA, Schulenburg H, Soluch R, Sommer F, Stukenbrock E, Weiland-Bräuer N, Rosenstiel P, Franke A, Bosch T, Baines JF (2019) Microbiome, doi: 10.1186/s40168-019-0743-1

2019
A2
A4
B1
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Neutrality in the metaorganism

Sieber M, Pita L, Weiland-Bräuer N, Dirksen P, Wang J, Mortzfeld B, Franzenburg S, Schmitz RA, Baines JF, Fraune S, Hentschel U, Schulenburg H, Bosch TCG, Traulsen A (2019) PLoS Biol., DOI: 10.1371/journal.pbio.3000298

2019
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Resolving structure and function of metaorganisms through a holistic framework 2 combining reductionist and integrative approaches

Jaspers C, Fraune S, Consortium of Australian Academy of Science Boden Research Conference Participants, Arnold AE, Miller DJ, Bosch TCG, Voolstra CR (2019) Zoology. doi: 10.1016/j.zool.2019.02.007

2019
B2

Potential role of host-derived quorum quenching in modulating bacterial colonization in the moon jellyfish Aurelia aurita

Weiland-Bräuer N, Pinnow N, Fischer MA, Schmitz RA (2019) Scientific Reports, 9(1), 34. DOI:10.1038/s41598-018-37321-z

2018
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B2
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Z2

Functions of the Microbiota for the Physiology of Animal Metaorganisms

Esser D, · Lange J, · Marinos G, · Sieber M, Best L, Prasse D, Bathia J, Rühlemann MC, Boersch K, Jaspers C, Sommer F (2018) J Innate Immun DOI: 10.1159/000495115

2018
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Metaorganisms in extreme environments: do microbes play a role in organismal adaptation?

Bang C, Dagan T, Deines P, Dubilier N, Duschl W J, Fraune S, Hentschel U, Hirt H, Hülter N, Lachnit T, Picazo D, Galan P L, Pogoreutz C, Rädecker N, Saad M M, Schmitz R A, Schulenburg H, Voolstra C R, Weiland-Bräuer N, Ziegler M, Bosch T C G (2018); Zoology, doi: 10.1016/j.zool.2018.02.004

2017
B2

Microbial contributions to the persistence of coral reefs.

Webster N S, Reusch T B H (2017); ISME J., doi: 10.1038/ismej.2017.66

2016
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B2

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 R A, Tholey A (2016)
J Proteome Res., 15(10):3773-3783. doi: 10.1021/acs.jproteome.6b00569

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