Function of the Woeseiaceae in marine sediments

A fingernail-sized piece of sea sand harbors more than a billion microorganisms. Although of similar appearance these are evolutionary very different and can also have very different life strategies. This makes marine sediment one of the microbially most diverse ecosystems on Earth. Despite this enormous diversity Dr. Mussmann and his team could recently identify one of the first bacterial families that thrives in virtually every marine sediment, including tropical beaches and the barren deep sea. The so-called Woeseiaceae have just recently been described and named after the famous pioneer of molecular evolution, Carl Woese. These bacteria are tiny but account for more than 10 million cells in that piece of sea sand. Because of their ubiquity and their high cell numbers they are expected to substantially impact element cycles in sediments worldwide. It is thus counterintuitive that the Woeseiaceae can hardly be grown and maintained in the laboratory to study their biology in detail. In this project Dr. Mussmann and his team aim at bypassing this obstacle and for the first time systematically study the function of Woeseiaceae in nature. They will apply modern genetic tools, sequencing of DNA and RNA recovered from the seafloor, which promises unprecedented insights into the actual function of these bacteria in sediments from distinct sites worldwide. Using powerful computers they will search for genomic DNA pieces of the Woeseiaceae and put them together, just like a jigsaw puzzle. Reading and interpreting this DNA puzzle will tell, why these bacteria are so successful in marine sediment and what they live from. First results suggest that the Woeseiaceae live well on sugars and proteins, while breathing oxygen and CO2 - just like human beings. But Woeseiaceae are special: it appears that some thrive also on hydrogen, sulfur, nitrite and rusty iron. Particularly important could be their still unconfirmed potential to produce laughing gas (N2O), another strong greenhouse gas. Therefore, the scientists will test, how the Woeseiaceae contribute to the release of greenhouse gases, both CO2 and N2O. Intriguingly, some members of these versatile bacteria may also help in protecting the biosphere by detoxifying poisonous sulfur compounds and trapping CO2. However, at this stage these hypotheses are just words in their DNA. Hence, it is essential to test in the laboratory, whether the Woeseiaceae let actions follow these words. The experimental research conducted in this project will profoundly improve our understanding of the multiple functions of the cryptic Woeseiaceae. Detailed knowledge on their diverging activities in releasing and trapping greenhouse gasses helps to assess the effects that these bacteria have on marine element cycles and all life on Earth.

Our research project focused on the Woeseiales, a group of bacteria that are amongst the most common microbial groups in global marine sediments. Despite their prevalence, little is known about their physiological traits that contribute to their success and ubiquity. Our goal was to gain a deeper understanding of their ecophysiology and ecological function using molecular tools. Through a comprehensive survey of samples from over 20 countries, we identified intertidal sediments in Normandy, France, and surprisingly, shark aquaria sediments from the Vienna Aqua Zoo, as sites with the highest relative sequence abundances of Woeseiales. By sequencing total nucleic acids from these sediments, we were able to assemble partial genomes from Woeseiales and compared with published data in the currently largest genome survey for this group. Here, discovered that they possess an unusually diverse metabolism. They may play a vital ecological role in recycling proteins from dead organisms, both on the seafloor and in the Vienna Aqua Zoo. While they may prefer breathing oxygen, they also survive in deeper sediments by breathing fumarate, sulfur compounds, and potentially iron, fueled by hydrogen gas as energy source. In our search for iron-respiring Woeseiales, we made a surprising discovery: Magnetite, a unique form of iron oxide, is prevalent in coastal sediments worldwide and is often colonized by electroactive bacteria. These bacteria can generate electricity and store the energy in magnetite for other bacteria that use it to fix CO2 for their growth, just like plants. This is the first time this cooperative lifestyle has been described in a natural environment. Our results contribute to a deeper understanding of the success of Woeseiales and their role in marine biogeochemical cycles.