Animal host control of beneficial bacteria

What keeps non-pathogenic microorganisms at bay? Despite our genome-based understanding of the metabolic capacities of microbial symbionts is steadily increasing, little is known about how the host controls and confines them. All the same, it is primal to know how the symbiont manipulates host physiology to stably associate with it. Invertebrates, the microbiome plays a fundamental role in the bidirectional axis that integrates the gut and central nervous system activities, but the mechanisms responsible for microbiota-nervous system interactions are largely unknown. Marine nematode-bacterium associations are exquisitly specific, i.e. only one bacterial species can associate to the surface of one nematode species. Additionally, the symbiont spatial organization on the host surface is exact and faithfully maintained throughout host and symbiont generations via epidermal glandular sensory organs.

In this research we want to understand (1) how the animal immune and nervous systems control the identity, number and spatial distribution of their beneficial bacteria and (2) what is the ecological and evolutionary significance of specific symbiosis “outfits” (i.e. bacterial coat architectures). We will address these questions by comparing transcriptomes of symbiotic vs non-symbiotic tissues, as well as those of four selected host species. Moreover, we will compare the transcriptomes and proteomes of the four corresponding symbionts. Upon employment of omics techniques, we will analyze the function of selected molecules such as host immune effectors and neuropeptides, or symbiont secretion systems. Moreover, omics data will be employed to predict host - symbiont molecular exchange via metabolic modeling.

Duration: 05.05.2016-04.05.2021

Funding agency: Austrian Science Fund (FWF)

Project leader: Dr. Silvia Bulgheresi

Participants: Silvia Bulgheresi, Jean-Marie Volland, Lena König, Tobias Viehböck, Friedrich Mössel

DK plus: Microbial Nitrogen Cycling

Duration: 01.01.2016-28.02.2021

Funding agency: Austrian Science Fund (FWF): W 1257

Project coordinator: Prof. Christa Schleper

Participants: Christa Schleper, Silvia Bulgheresi, Melina Kerou, Logan Hodgskiss, Gabriela Paredes, Michael Melcher, Philipp Weber, Carolina Reyes

Project webpage: DK+ Microbial Nitrogen Cycling

Marine nematode symbioses

Stilbonematids (Desmodoridae, Chromadoria) are marine nematodes coated with sulfur-oxidizing bacteria. They are the only known marine metazoans capable of establishing monospecific ectosymbioses. Hundreds of highly specialized hypodermal glandular sensory organs (GSOs) appear to play a fundamental role in symbiosis establishment and maintenance: they produce the mucus the symbionts are embedded in.
In the course of our ongoing research project, we want to study abundantly expressed stilbonematid genes discovered by pyrosequencing-based transcriptome analysis. Among these, some are secreted by the GSOs onto the worm's surface and might play a role in symbiosis. In order to understand their function, we will analyze their expression pattern within the GSO and try to silence them by RNA interference.
Concomitantly, we will start to explore how the microbial partners manage to divide without loosing physical contact with their hosts. This requires a highly unusual division mode in which the fission plan is set longitudinally to the symbiont long axis.

The study of relatively simple, naturally occurring symbioses may be instrumental in understanding how beneficial and pathogenic microbes interact with the mucosal surfaces of higher vertebrates.

Growth and septation of animal-attached bacteria

Bacterial cell growth and division have only been studied in a dozen of cultivable species in spite of the fact that millions of them are estimated to live on our planet. This knowledge gap must be urgently filled if we want to grasp the conserved fundamentals of cell reproduction. Therefore, we studied the reproductive strategies of Thiosymbion, a group of non-model bacteria, which exclusively occur on the surface of animals (ectosymbionts). In particular, in longitudinally dividing Thyiosymbion, we found that: 1) septation can start at one cell pole only, so that a ring of the tubulin homolog FtsZ is dispensable; 2) not only bacterial cell division but also cell growth can be host-polarised; 3) the actin homolog MreB is medial throughout the cell cycle and its polymerisation is required for medial FtsZ polymerisation and septation; 4) a bidimensional segregation mode maintains symbiont chromosome orientation toward it host. We hypothesise that these extraordinary cell biological features are adaptions to the symbiotic lifestyle. Establishment of symbiont cultures and development of gene manipulation/protein imaging techniques are ongoing to prove that cell biological adaptations, such as longitudinal division or fixed chromosome configuration, are required for symbiosis establishment or maintenance.

Publications from this project:

Pende N, Wang J, Weber P, Verheul J, Kuru E, Rittmann S..... Bulgheresi S, (2018). Host-Polarized Cell Growth in Animal Symbionts.. Current biology : CB, 28 (7), pp. 1039-1051.e5
DOI: 10.1016/j.cub.2018.02.028
pubmed.ncbi.nlm.nih.gov/29576473/

Weber P, Moessel F, Paredes G, Viehboeck T, Vischer N, Bulgheresi S, (2019). A Bidimensional Segregation Mode Maintains Symbiont Chromosome Orientation toward Its Host.. Current biology : CB, 29 (18), pp. 3018-3028.e4
DOI: 10.1016/j.cub.2019.07.064
www.sciencedirect.com/science/article/pii/S0960982219309443

Leisch N, Pende N, Weber PM, Gruber-Vodicka HR, Verheul J, Vischer NO, Abby SS... Bulgheresi S. (2016). Asynchronous division by non-ring FtsZ in the gammaproteobacterial symbiont of Robbea hypermnestra.. Nature microbiology, pp. 16182
DOI: 10.1038/nmicrobiol.2016.182
www.nature.com/articles/nmicrobiol2016182