Microbial symbiosis

SYMBIOSIS

 

All multicellular organisms have evolved in environments long inhabited by bacteria and therefore they had to evolve with, and in response to, microorganisms. In consequence, symbiosis with microbes is the norm rather than the exception in multicellular organisms. Symbiosis is broadly defined as the “living together of two unlike organism”, and ranges from highly specific partnerships (1 host – 1 symbiont) to complex, multi-species associations (e.g. the microbiome inhabiting the human gut). We study relatively simple invertebrate systems to understand the basic principles for the evolution and function of symbiosis.

 

 

Bacterial Symbionts of Earthworms

Earthworms have species-specific symbiotic bacteria in their excretory organs (nephridia). During the past decade we have been investigating the evolution and function of the most common symbiont, Verminephrobacter. The ability to separate host and symbiont in the lab gives us an experimental system where we can compare life-history and physiological traits in worms with and without symbionts, and also study symbiont physiology in detail using omics approaches. We could show that Verminephrobacter increase host reproductive success and thus are beneficial for earthworms. Our current research focuses on the underlying functional mechanism, and on the role of secondary and tertiary symbionts in certain worm species.

 

 

Symbiosis in Marine Invertebrates

Most marine invertebrates host microbial symbionts that can have diverse beneficial functions, e.g. provide them with energy, carbon, vitamins and co-factors, protection against predation or harmful bacteria, or waste removal. We explore understudied animal groups and have discovered specific bacterial symbionts in Xenoturbella, Priapulus, and several ascidians (Tunicata, Ascidiacea), and currently focus on phylogeny, physiology, and function of Endozoicomonas, a bacterial lineage always found in association with marine invertebrates. 

 

 

Genome Evolution in Symbiosis

Long-term stable host associations result in a marked impact on symbiont genome evolution. The “standard model” for intracellular symbionts predicts successive loss of genes and genome erosion, leading to the smallest prokaryotic genomes known. In contrast, there is no consensus model for genome evolution in extracellular symbionts but increased mutation rates and massive shuffling of gene order have been observed. We use the vertically transmitted earthworm symbionts Verminephrobacter that have co-evolved with their host for about 100 million years, and the presumably horizontally transmitted marine symbionts Endozoicomonas as contrasting model systems for genome evolution in extracellular symbionts. One key question is the role of genetic exchange within symbiont populations (by homologous recombination) and the acquisition of new genes from other organisms (by horizontal gene transfer) for maintaining genome integrity.

 

 

Key Publications

 

Lund MB, Kjeldsen KU, Schramm A. (2014). The earthworm-Verminephrobacter symbiosis: an emerging experimental system to study extracellular symbiosis. Front Microbiol 5.

 

Kjeldsen KU, Bataillon T, Pinel N, De Mita S, Lund MB, Panitz F, Bendixsen C, Stahl DA, Schramm A. (2012). Purifying selection and molecular adaptation in the genome of Verminephrobacter, the heritable symbiotic bacteria of earthworms. Gen Biol Evol 4:307–315.

 

Kjeldsen KU, Obst M, Nakano H, Funch P, Schramm A. (2010). Two types of endosymbiotic bacteria in the enigmatic marine worm Xenoturbella. Appl. Environ. Microbiol 76: 2657-2662 (cover image: aem.asm.org/content/76/8.cover-expansion)

 

 

Lund MB, Davidson SK, Holmstrup M, James S, Kjeldsen KU, Stahl DA, Schramm A. (2010). Diversity and host specificity of the Verminephrobacter-earthworm symbiosis. Environ Microbiol 12:2142–2151.

 

Lund MB, Holmstrup M, Lomstein BA, Damgaard C, Schramm A. (2010). Beneficial effect of Verminephrobacter nephridial symbionts on the fitness of the earthworm Aporrectodea tuberculata. Appl Environ Microbiol 76:4738–4743.

 

Schramm A, Davidson SK, Dodsworth JA, Drake HL, Stahl DA, Dubilier N. (2003). Acidovorax-like symbionts in the nephridia of earthworms. Environ Microbiol 5:804–809. (cover image: onlinelibrary.wiley.com/doi/10.1111/emi.2003.5.issue-9/issuetoc)

Verminephrobacter symbionts (red) inside earthworm nephridium (green).
Ascidia virginea, a solitary ascidian with specific bacterial symbionts (picture by Peter Funch)
Schematic of two genomes of Verminephrobacter eiseniae (left) and V. aporrectodeae (right) where shared genes are connected by lines. There is no conserved gene order (synteny) between the symbionts, which is unusual for closely related bacteria.

 

 

EU Marie Curie Initial Training Networks (ITN) “SYMBIOMICS

The Danish Council for Independent Research | Natural Sciences (FNU)

Danish Agency for Science, Technology and Innovation

Aarhus Institute of Advanced Studies (AIAS)

Aarhus University Research Foundation

EU Association of European Marine Biological Laboratories (ASSEMBLE)