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Life without a mouth, stomach, or gut

How a small worm gets by with a little help from its bacteria
 
No one is alone: All living organisms are inhabited by a complex community of beneficial microorganisms that are essential for their development, health, and interactions with the environment. Often these microorganisms protect their hosts against harmful bacteria, such as the microbial community of the human skin. Other microorganisms are essential for their hosts because they either help them digest their food or provide them with nutrition directly. In return, the host offers its bacterial community a stable and secure place to live. These mutually beneficial associations are called symbioses.

The study of symbioses is often challenging because most symbiotic microorganisms can not be isolated from their host. Only recently have genomic analyses provided insight in the complex interactions and cross-talk that occur between hosts and their symbionts. To date, these types of analyses have been largely limited to simple systems with only a single symbiotic species. Scientists from the Bremen Max Planck Institute for Marine Microbiology and the Joint Genome Institute in the USA have now successfully unraveled the genomes of a complex community of four bacterial symbionts that live inside the marine worm Olavius algarvensis using so-called metagenomic analyses. This study represents the largest genomic dataset of a symbiotic community and provides an important basis for the analysis of other complex symbioses, such as the human gut microbiota. This work was conducted by a team of scientists at the Bremen Max Planck Institute led by Dr. Nicole Dubilier and by Dr. Tanja Woyke and colleagues from the Joint Genome Institute led by the JGI director, Dr. Eddy Rubin.
Left: Olavius algarvensis under the microscope (MPI Bremen and Hydra Institute, Elba, C. Lott). Middle: Divers collect the worms from sands around sea grass beds off the coast of the Mediterranean island of Elba (MPI Bremen and Hydra Institute, Elba, M. Weber). Right: The Bay of Sant’ Andrea on Elba where the worms are found (MPI Bremen and Hydra Institute, Elba, C. Lott).
Olavius algarvensis is a marine oligochaete that lives in the upper 20 centimeters of shallow-water sands off the coast of the Mediterranean island of Elba. The scientist Dr. Nicole Dubilier from the Bremen Max Planck Institute for Marine Microbiology together with colleagues from her Symbiosis Group have been working for years on the symbioses of marine oligochaetes. The anatomy of these worms is particularly unusual because they not only lack a mouth, stomach, and gut, but also nephridia, kidney-like organs. While the reduction of the digestive system also occurs in other animals groups, these worms are the only hosts that have also reduced their excretory system as an adaptation to the symbiosis. For the worms, this means that their symbionts are responsible for both providing them with food and removing their waste compounds. The metagenomic analyses revealed how these essential host tasks could be delegated to the symbionts, a wonderful example for outsourcing of energy and waste management.

Metagenomic analyses: How newly developed computing methods helped the scientists
The genome is the total complement of genes in an organism. In classical genomic analyses, the genetic material of a single species is sequenced using well established methods and every year hundreds of new genomes are published by scientists and deposited in the databases. These classical analyses do not, however, work for samples containing a mixture of species because they do not allow an assignment of the sequences to the species from which they originated. For the study of microbial communities metagenomic analyses are used. The metagenome is defined as the total complement of all genes in an environmental sample.

One of the major challenges in metagenomics is assigning the mixture of genomic sequences from an environmental sample to a given species. This problem can be illustrated with an example from text analyses. Imagine a hopeless mess of books from different authors with the texts broken up in bits and pieces. These must be put back together in their original form. As every author has his or her own unique style of writing, the original texts can be reconstructed by statistically analyzing the text fragments. In genomic “texts”, however, there are only four letters, A, G, C, and T. And these letters are not separated by dots or commas. Dr. Hanno Teeling from the Microbial Genomics Group of Prof. Dr. Frank Oliver Glöckner was able to solve this problem by developing a new mathematical algorithm for so-called binning analyses. The relative frequency of all 64 possible triplets of A,G,C, and T, all 256 possible quadruplets of these four base pairs, and the frequency of G and C in a defined genomic sequence differs distinctly between species. These unique signatures were used to separate the genomic fragments into distinct groups, so-called bins. These fragments were then assembled and annotated, allowing the reconstruction of the genomes of the four symbionts of O. algarvenis. This enabled the scientists to reconstruct the metabolism of the symbionts and revealed which pathways are used under different environmental conditions.

What was found?

Two sulfur bacteria (Gammaproteobacteria) and 2 sulfate reducers (Deltaproteobacteria) co-occur in the worm. The sulfate reducers produce reduced sulfur compounds that can be used by the sulfur bacteria to gain energy, so that the symbionts feed each other in a syntrophic sulfur cycle. Surprisingly, all four symbionts can fix carbon dioxide as plants do, making these worms comparable to an endosymbiotic power plant. The four symbionts are also involved in the detoxification of poisonous waste products such as urea and ammonium and thus contribute to the recycling of valuable nitrogen.

Outlook

This little worm shows how the coordinated interaction of its microbial community enables it to efficiently use limited resources in a confined space. This makes the Olavius symbiosis a model for a nearly self-sufficient biosphere. Comparable systems on a much larger scale are currently being studied intensively. These are interesting for long interplanetary space travels, such as the planned flight to Mars.
Reference
Tanja Woyke, Hanno Teeling, Natalia N. Ivanova, Marcel Hunteman, Michael Richter, Frank Oliver Gloeckner, Dario Boffelli, Iain J. Anderson, Kerrie W. Barry, Harris J. Shapiro, Ernest Szeto, Nikos C. Kyrpides, Marc Mussmann, Rudolf Amann, Claudia Bergin, Caroline Ruehland, Edward M. Rubin, Nicole Dubilier
Symbiosis insights through metagenomic analysis of a microbial consortium, NATURE, September 2006.

Press releases:
Joint Genome Institute press release:
http://www.jgi.doe.gov/News/news_9_18_06.html

Max Planck Society press release:
http://www.mpg.de/bilderBerichteDokumente/dokumentation/pressemitteilungen/2006/pressemitteilung20060918/index.html

Requests:
Dr. Nicole Dubilier
+49 421 2028 932 [Bitte aktivieren Sie Javascript]
Max Planck Institute for Marine Microbiology, Bremen 28359, Germany

Dr. Manfred Schlösser ( Press Officer)
+49 421 2028 704 [Bitte aktivieren Sie Javascript]
Max Planck Institute for Marine Microbiology, Bremen 28359, Germany

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