Vertical segregation and phylogenetic characterization of ammonia-oxidizing Archaea in a deep oligotrophic lake

Abstract

Freshwater habitats have been identified as one of the largest reservoirs of archaeal genetic diversity, with specific lineages of ammonia-oxidizing archaea (AOA) populations different from soils and seas. The ecology and biology of lacustrine AOA is, however, poorly known. In the present study, vertical changes in archaeal abundance by CARD-FISH, quantitative PCR (qPCR) analyses and identity by clone libraries were correlated with environmental parameters in the deep glacial high-altitude Lake Redon. The lake is located in the central Spanish Pyrenees where atmospheric depositions are the main source of reactive nitrogen. Strong correlations were found between abundance of thaumarchaeotal 16S rRNA gene, archaeal amoA gene and nitrite concentrations, indicating an ammonium oxidation potential by these microorganisms. The bacterial amoA gene was not detected. Three depths with potential ammonia-oxidation activity were unveiled along the vertical gradient, (i) on the top of the lake in winter–spring (that is, the 0 oC slush layers above the ice-covered sheet), (ii) at the thermocline and (iii) the bottom waters in summer—autumn. Overall, up to 90% of the 16S rRNA gene sequences matched Thaumarchaeota, mostly from both the Marine Group (MG) 1.1a (Nitrosoarchaeum-like) and the sister clade SAGMGC−1 (Nitrosotalea-like). Clone-libraries analysis showed the two clades changed their relative abundances with water depth being higher in surface and lower in depth for SAGMGC−1 than for MG 1.1a, reflecting a vertical phylogenetic segregation. Overall, the relative abundance and recurrent appearance of SAGMGC−1 suggests a significant environmental role of this clade in alpine lakes. These results expand the set of ecological and thermal conditions where Thaumarchaeota are distributed, unveiling vertical positioning in the water column as a key factor to understand the ecology of different thaumarchaeotal clades in lacustrine environments.

Contrasting taxonomic stratification of microbial communities in two hypersaline meromictic lakes

“…Ammonium reached the highest concentrations in the deep anoxic layers of the lakes, indicating a higher rate of mineralization than assimilation, coupled with a higher stability in the acidic pH range. The depth profiles of ammonium concentration were comparable for both Ursu and Fara Fund lakes, and similar to the ones described in other stratified lakes (Auguet et al, 2012;La Cono et al, 2013;Yau et al, 2013). The vertical profiles of nutrients (sulfate, sulfide, nitrite, nitrate and phosphate) were found to be a result of sedimentation, biogeochemical cycling or conservative mixing (Pasche et al, 2009), and were also comparable with those found in other studied lakes (Lepère et al, 2010;La Cono et al, 2013;Marteinsson et al, 2013).…”

Conversion of upland to paddy field specifically alters the community structure of archaeal ammonia oxidizers in an acid soil

“…This finding agrees well with our results, indicating that AOA community diversification might be attributed to variations in oxygen availability and other environmental 5749 factors upon conversion of upland to flooded paddy soil. The predominance of AOA communities was indeed frequently observed in oxygen minimum zones of marine environments (Beman et al, 2008;Bouskill et al, 2012) and oligotrophic lake waters (Herrmann et al, 2008;Auguet et al, 2012). In a highly aerated sludge with high concentrations of dissolved oxygen, AOA abundance was at least three orders of magnitude lower than that of AOB (Wells et al, 2009).…”

Insights in the ecology and evolutionary history of the Miscellaneous Crenarchaeotic Group lineage

“…Although a comprehensive phylogeny subdividing the MCG lineage into 17 monophyletic subgroups has recently been reported (Kubo et al, 2012), many questions remain unanswered concerning the distribution and functions of these subgroups in the different habitats. Of particular interest is the ability of MCG to overcome one of the most important evolutionary barriers structuring microbial communities, that is, salinity Lozupone and Knight, 2007) and to colonize both marine and freshwater habitats (Casamayor et al, 2001;Biddle et al, 2006;Lehours et al, 2007;Llirós et al, 2008Llirós et al, , 2010Auguet et al, 2010Auguet et al, , 2012Bhattarai et al, 2012;Borrel et al, 2012;Buckles et al, 2013;Fillol et al, 2015). In addition to the fact that the abundance of MCG in freshwater habitats is still not well estimated, no study has yet been conducted to investigate the evolutionary relationships between marine and freshwater MCG, and whether or not distinct MCG subgroups have evolved along the transition between marine and freshwater habitats.…”