Distribution and activity of chemolithoautotrophic microorganisms in Baltic pelagic redoxclines
Final Report Abstract
Stable stratified aquatic habitats are often characterized by a separation of their water column into oxic upper water and hypoxic, often also sulfidic, bottom water. The redox gradient between these environments is referred to as a pelagic redoxcline. The redoxcline is governed by a complex matrix of biogeochemical processes mostly related to sulfur, oxygen, nitrogen, carbon but also to the cycling of metals. One characteristic feature which can be observed in suboxic to sulfidic transition zones of pelagic redoxclines are considerably high CO2 fixation rates, in consequence usually coupled to higher abundances auf autotrophic microorganisms. In systems located below the photic layer mostly aerobic as well as anaerobic dark CO2 fixing (chemolithoautotrophic) microorganisms have been proposed to be responsible for the observed fixation rates. Despite this significant impact, the knowledge about respective chemolithoautotrophic assemblages was still low. Especially knowledge on physiological properties, but also the identity and diversity of chemolitoautotrophic assemblages was restricted. Thus, aim of the projects was to discover the diversity, ecology, and physiology of chemolithoautrophic microorganisms and their role in nutrient cycling. This was predominantly done for pelagic redoxclines of the central Baltic Sea, but complemented by Black Sea analyses. Research highlights are: The importance of chemolithoautotrophic bacteria in pelagic redoxclines, accounting for up to 40 % of total prokaryotes, was recognized. For the first time, using methods linking structure and function of prokaryotes, the successful identification of a chemolithoautotrophic, bacterial key player was provided for marine pelagic redoxclines. Cells of this nitratereducing key player (genus Sulfurimonas, named “subgroup GD17”) contributed in cellular abundances more than 70 % of total chemoautotrophs. In general it was remarkable that, despite high abundances of chemolithoautotrophic assemblages in anoxic zones, their diversity was low and restricted to a few epsilon- and gammaproteobacterial organisms. A close relative of the GD17 subgroup, “Sulfurimonas gotlandica” str. GD1, was isolated from a central Baltic Sea redoxcline. This fact enabled a detailed and complementary study of its genome and its physiology in laboratory experiments. Based on GD1 laboratory studies it could be shown that this denitrifying key organism is able to gain energy by the anaerobic oxidation of sulfide, sulfur, thiosulfate, and sulfite. It is characterized by a high metabolic flexibility, suggesting a considerable capacity for adaptation to variable redox conditions and it is very probable that the whole GD17 subgroup exhibits these capabilities in vivo. Concerning other important parts of the nitrogen cycle it was discovered that, analogous to autotrophic denitrification, also aerobic ammonium oxidation was catalyzed by a much less diverse microbial community than described for principally comparable habitats as, e.g., the Black Sea: nitrifying populations throughout pelagic redoxclines in the central Baltic Sea consisted only of one thaumarchaeal subcluster, named GD2, which was closely related to Candidatus Nitrosopumilus maritimus. This was the first time to show the dominance of one thaumarchaeal nitrifying key cluster in a natural habitat. It is assumed that local mixing events transferring sulfide-rich water masses into suboxic zones of pelagic redoxclines could favor ammonia-oxidizing archaea, because the inhibitory effect of sulfide or other S-containing compounds is more severe on bacterial than on archaeal nitrification. To summarize, it can be concluded that especially the N-cycle in pelagic central Baltic Sea redoxclines is driven by only a few key organisms, supporting only a limited amount of nitrogen transformation pathways and, consequently, could serve as a simple model for microbially catalyzed N-cycling. Taken this, we postulate that, due to the natural abundance and cultivability of ´Sulfurimonas gotlandica´ str. GD1, this isolate is a suitable model organism for understanding the ecological impact of these organisms in expanding hypoxic/sulfidic areas in the oceans worldwide.
Publications
- (2007). Distribution of abundant prokaryotic organisms in the water column of the central Baltic Sea with an oxic-anoxic interface. Aquatic Microbial Ecol 46, 177-190
Labrenz, M., Jost, G. & Jürgens, K.
- (2007). Quantitative distribution of Epsilonproteobacteria and a specific Sulfurimonas subgroup in pelagic redoxclines of the central Baltic Sea. Appl Environ Microbiol 73, 7155-7161
Grote, J., Labrenz, M., Pfeiffer, B., Jost, G. & Jürgens, K.
- (2008). High abundance and dark CO2 fixation of chemolithoautotrophic bacteria in anoxic waters of the Baltic Sea. Limnol Oceanogr 53, 14-22
Jost, G., Zubkov, M. V., Yakushev, E., Labrenz, M. & Jürgens, K.
- (2008). Significant chemoautotrophic activity of Epsilonproteobacteria in marine pelagic redoxclines as determined by MICRO-CARD-FISH. Appl Environ Microbiol, 74 7546-7551
Grote, J., Jost, G., Labrenz, M., Herndl, G. & Jürgens, K.
- (2009). C-isotope analyses reveal that chemolithoautotrophic Gamma- and Epsilonproteobacteria feed a microbial food web in a pelagic redoxcline of the central Baltic Sea. Environ Microbiol 11, 326-337
Glaubitz, S., Lueders, T., Abraham, W.-R., Jost, G., Jürgens, K. & Labrenz, M.
- (2010). Anaerobic sulfur oxidation in the absence of oxygen and nitrate dominates microbial chemoautotrophy beneath the pelagic chemocline of the Eastern Gotland Basin, Baltic Sea. FEMS Microbiol Ecol 71, 226-236
Jost, G., Martens-Habbena, W., Pollehne, F., Schnetger, B., & Labrenz, M.
- (2010). Diversity of active chemolithoautotrophic prokaryotes in the sulfidic zone of a Black Sea pelagic redoxcline as determined by rRNA-based stable isotope probing. FEMS Microbiol Ecol 74, 32–41
Glaubitz, S., Labrenz, M., Jost, G., & Jürgens, K.
- (2010). Relevance of a crenarchaeotal subcluster related to Candidatus Nitrosopumilus maritimus to ammonia oxidation in the suboxic zone of the central Baltic Sea. ISME J 4, 1496-1508
Labrenz, M., Sintes, E., Toetzke, F., Zumsteg, A., Herndl, G. J., Seidler, M., Jürgens, K.
