Evolution and niche separation of culturable anaerobic prokaryotes in hypersaline microbial mats and sediments
PI: Dr. Stefan Spring
Some hypersaline lakes on the Kiritimati Atoll are characterized by photosynthetically active mats that are several thousand years old and form microbialites below the growth zone. They represent an interesting model ecosystem that differs from most known stromatolites, which calcify in the upper layers.
The hypersaline mats are composed mainly of cyanobacteria in the upper layers and anaerobic bacteria in the deeper zones where the mineralization takes place (Fig. 1). While cyanobacteria represent the main primary producers, the function of the non-phototrophic microbial community is largely unknown, but it is thought that distinct types of Bacteria and Archaea play a major role in the precipitation of minerals. In the course of this research project we could isolate a large number of novel strains from the anoxic zone of the photosynthetically active mat of the Kiritimati Lake 21 .
Especially, fermentative bacteria were present in large numbers and high diversity. For comparison additional anaerobic heterotrophic isolates were obtained from saline sediments of evaporation ponds in Portugal and Spain. We now try to define the ecological niche and putative function of these strains in hypersaline ecosystems by using traditional phenotypic methods and genome sequencing as well as determination of cultivation independent environmental data. For example, it turned out that an isolate affiliated with a novel Bacteroidetes clade shows a distinct niche specialization within the mat and seems to be involved in the degradation and recycling of cyanobacterial biomass . Furthermore, comparative genome analyses revealed several adaptations of fermentative microorganisms to hypersaline microbial mats. First, the competition among strains inhabiting the same niche seems to be reduced, which leads to relaxed genome structures with a high prevalence of mobile elements and non-functional pseudo genes. Second, stress factors within the mat seem to have a large impact on genome stability thereby causing probably high mutation rates that in turn maybe advantageous under rapidly changing environmental conditions .
In addition to fermentative bacteria, high numbers of sulfate-reducing and respiratory microorganisms were detected in deeper layers of the mat using cultivation-independent methods. Of particular interest was a novel isolate assigned to the family Desulfovibrionaceae that is restricted to a specific layer of the suboxic zone characterized by the presence of aragonitic spherulites . In addition, a nitrate-reducing bacterium from the class Deferribacteres was isolated and characterized in detail. The combination of metabolome and genome studies revealed a potentially new mechanism of nitrite reduction that provides more energy than the conventional pathway, which could be crucial under energy-limiting conditions in hypersaline microbial mats .
Spring, S., Brinkmann, N., Murrja, M., Spröer, C., Reitner, J., Klenk, H.-P. (2015) High diversity of culturable prokaryotes in a lithifying hypersaline microbial mat. Geomicrobiol. J. 32 (3-4):332-346 .
Ben Hania, W., Joseph, M., Bunk, B., Spröer, C., Klenk, H.-P., Fardeau, M.-L., Spring, S. (2017) Characterization of the first cultured representative of a Bacteroidetes clade specialized on the scavenging of cyanobacteria. Environ. Microbiol. 19:1134–1148.
Spring, S., Bunk, B., Spröer, C., Rohde, M., Klenk, H.-P. (2018) Genome biology of a novel lineage of planctomycetes widespread in anoxic aquatic environments. Environ. Microbiol. 20: 2438-2455 .
Spring, S., Sorokin, D. Y., Verbarg, S., Rohde, M., Woyke, T., Kyrpides, N. C. (2019) Sulfate-reducing bacteria that produce exopolymers thrive in the calcifying zone of a hypersaline cyanobacterial mat. Front. Microbiol. 10:862.
Spring, S., Rohde, M., Bunk, B., Spröer, C., Will, S.E. and Neumann-Schaal, M. (2022) New insights into the energy metabolism and taxonomy of Deferribacteres revealed by the characterization of a new isolate from a hypersaline microbial mat. Environ. Microbiol. 24: 2543-2575..