Bacteria have important roles in freshwater food webs and in the cycling of elements in the ecosystem. Yet specific ecological features of individual phylogenetic groups and interactions among these are largely unknown. We used 454 pyrosequencing of 16S rRNA genes to study associations of different bacterioplankton groups to environmental characteristics and their co-occurrence patterns over an annual cycle in a dimictic lake. Clear seasonal succession of the bacterioplankton community was observed. After binning of sequences into previously described and highly resolved phylogenetic groups (tribes), their temporal dynamics revealed extensive synchrony and associations with seasonal events such as ice coverage, ice-off, mixing and phytoplankton blooms. Coupling between closely and distantly related tribes was resolved by time-dependent rank correlations, suggesting ecological coherence that was often dependent on taxonomic relatedness. Association networks with the abundant freshwater Actinobacteria and Proteobacteria in focus revealed complex interdependencies within bacterioplankton communities and contrasting linkages to environmental conditions. Accordingly, unique ecological features can be inferred for each tribe and reveal the natural history of abundant cultured and uncultured freshwater bacteria.

Despite the high abundance of Archaea in the global ocean, their metabolism and biogeochemical roles remain largely unresolved. We investigated the population dynamics and metabolic activity of Thaumarchaeota in polar environments, where these microorganisms are particularly abundant and exhibit seasonal growth. Thaumarchaeota were more abundant in deep Arctic and Antarctic waters and grew throughout the winter at surface and deeper Arctic halocline waters. However, in situ single-cell activity measurements revealed a low activity of this group in the uptake of both leucine and bicarbonate (<5% Thaumarchaeota cells active), which is inconsistent with known heterotrophic and autotrophic thaumarchaeal lifestyles. These results suggested the existence of alternative sources of carbon and energy. Our analysis of an environmental metagenome from the Arctic winter revealed that Thaumarchaeota had pathways for ammonia oxidation and, unexpectedly, an abundance of genes involved in urea transport and degradation. Quantitative PCR analysis confirmed that most polar Thaumarchaeota had the potential to oxidize ammonia, and a large fraction of them had urease genes, enabling the use of urea to fuel nitrification. Thaumarchaeota from Arctic deep waters had a higher abundance of urease genes than those near the surface suggesting genetic differences between closely related archaeal populations. In situ measurements of urea uptake and concentration in Arctic waters showed that small-sized prokaryotes incorporated the carbon from urea, and the availability of urea was often higher than that of ammonium. Therefore, the degradation of urea may be a relevant pathway for Thaumarchaeota and other microorganisms exposed to the low-energy conditions of dark polar waters.amoA | ureC | Beaufort Sea | Ross Sea | Amundsen Sea

The aquatic bacterial group SAR11 is one of the most abundant organisms on Earth, with an estimated global population size of 2.4 Â 10 28 cells in the oceans. Members of SAR11 have also been detected in brackish and fresh waters, but the evolutionary relationships between the species present in the different environments have been ambiguous. In particular, it was not clear how frequently this lineage has crossed the saline-freshwater boundary during its evolutionary diversification. Due to the huge population size of SAR11 and the potential of microbes for long-distance dispersal, we hypothesized that environmental transitions could have occurred repeatedly during the evolutionary diversification of this group. Here, we have constructed extensive 16S rDNA-based molecular phylogenies and undertaken metagenomic data analyses to assess the frequency of saline-freshwater transitions in SAR11 and to investigate the evolutionary implications of this process. Our analyses indicated that very few saline-freshwater transitions occurred during the evolutionary diversification of SAR11, generating genetically distinct saline and freshwater lineages that do not appear to exchange genes extensively via horizontal gene transfer. In contrast to lineages from saline environments, extant freshwater taxa from diverse, and sometimes distant, geographic locations were very closely related. This points to a rapid diversification and dispersal in fresh waters or to slower evolutionary rates in fresh water SAR11 when compared with marine counterparts. In addition, the colonization of both saline and fresh waters appears to have occurred early in the evolution of SAR11. We conclude that the different biogeochemical conditions that prevail in saline and fresh waters have likely prevented the environmental transitions in SAR11, promoting the evolution of clearly distinct lineages in each environment.

THE SAR11 clade is ubiquitous and abundant in planktonic environments. In freshwater lakes, the clade is represented by tribe LD12 which is phylogenetically distinct from the marine SAR11. We studied the ecology of LD12 in a temperate dimictic lake (Lake Erken, Sweden), by analyzing its seasonal dynamics with quantitative PCR, CARD-FISH and 454 pyrosequencing of the 16S rRNA gene. Results showed that LD12 can be as numerous in freshwater bacterioplankton as their marine SAR11 siblings. They exhibited strong seasonality and made up from 1.8 to 40% of the total bacterial 16S rRNA pool (mean 14%) with pronounced peaks in summer and late fall. Except in spring, LD12 was the dominant Alphaproteobacteria, contributing on average 72% of the 16S rRNA within this class. The LD12 population was dominated by a single persistent ribotype, suggesting low local divergence, at least at the phylogenetic resolution accessed with rRNA genes. The relative abundance of LD12 was positively correlated to nutrient concentrations (phosphate, ammonia, nitrate, and silica) and water transparency whereas the relative abundance was lower during periods characterized by high phytoplankton biomass. Based on these observations we propose that LD12 are poor competitors during periods of high phytoplankton productivity and associated release of labile organic compounds, but thrive when availability of inorganic nutrients is high. Similar to the marine SAR11 sibling group, local LD12 populations appear to respond in contrasting ways to nutrient availability in different lakes, pointing to either ecological divergence within the tribe or variations in the interplay between environmental driver variables.

Archaea are abundant in polar oceans but important ecological aspects of this group remain enigmatic, such as patterns of diversity and biogeography. Here, we provide the first high-throughput sequencing population study of Antarctic archaea based on 198 bp fragments of the 16S rRNA gene, targeting different water masses across the Amundsen and Ross Seas. Our results suggest that archaeal community composition is strongly shaped by hydrography and significantly influenced by environmental parameters. Archaeal communities from cold continental shelf waters (SW) of the Ross Sea were similar over depth with a single thaumarchaeal phylotype dominating Antarctic surface waters (AASW) and deeper SW (contributing up to 80% of reads). However, this phylotype contributed less than 8% of reads in circumpolar deep waters (CDW). A related thaumarchaeon (98% identity) was almost absent in AASW, but contributed up to 30% of reads in CDW, suggesting ecological differentiation of closely related phylotypes. Significantly higher archaeal richness and evenness were observed in CDW, with Shannon indices (c. 2.5) twice as high as for AASW, and high contributions of Group II Euryarchaeota. Based on these results, we suggest that CDW is a hotspot of archaeal diversity and may play an important role in the dispersal of archaeal phylotypes to other oceanic water masses.