Ubiquity and quantitative significance of bacterioplankton lineages inhabiting the oxygenated hypolimnion of deep freshwater lakes

Abstract

Freshwater bacterioplankton in the oxygenated hypolimnion are reportedly dominated by specific members that are distinct from those in the epilimnion. However, no consensus exists regarding the ubiquity and abundance of these bacterioplankton, which is necessary to evaluate their ecological importance. The present study investigated the bacterioplankton community in the oxygenated hypolimnia of 10 deep freshwater lakes. Despite the broad geochemical characteristics of the lakes, 16S rRNA gene sequencing demonstrated that many predominant lineages in the hypolimnion were shared by several lakes and consisted of members occurring in the entire water layer and members specific to the hypolimnion. Catalyzed reporter deposition fluorescence in situ hybridization (CARD-FISH) revealed that representative hypolimnion-specific lineages, CL500-11 (Chloroflexi), CL500-3, CL500-37, CL500-15 (Planctomycetes), and the MGI group (Thaumarchaeota), together accounted for 1.5-32.9% of all bacterioplankton in the hypolimnion of the lakes. Furthermore, an analysis of micro-diversification based on single-nucleotide variation in the partial 16S rRNA gene sequence (oligotyping) suggested the presence of hypolimnion-specific ecotypes among the lineages occurring in the entire water layer (e.g., acI and Limnohabitans). Collectively, these results demonstrate the uniqueness, ubiquity, and quantitative significance of bacterioplankton in the oxygenated hypolimnion, motivating future studies to focus on their eco-physiological characteristics.

Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake

“…Forty‐five (78.9%) of these genomes were of high quality, with estimated completeness and contamination scores of >80% and < 5%, respectively (Supporting Information Table S3). Consistent with previous observations (Okazaki and Nakano, ; Okazaki et al ., ), a depth‐stratified bacterioplankton community was observed – members of LD12, Actinobacteria and Cyanobacteria were dominant in the epilimnion, whereas CL500‐11 and Ca . Nitrosoarchaeum were dominant in the hypolimnion (Supporting Information Table S4).…”

“…), which is a member of the ammonia‐oxidizing, chemoautotrophic archaeal taxon Marine Group I (MGI). Members of MGI dominate the hypolimnion of deep freshwater lakes (Okazaki et al ., ) (Supporting Information Table S4) and thus are important players in the nitrogen and carbon cycles of lakes. In marine systems, members of MGI are also dominant in the deep aphotic layer, and recent studies have reported the presence of several putative MGI viruses (Chow et al ., ; Labonté et al ., ), including those encoding AMGs such as amoC (Ahlgren et al ., ) and cobS (López‐Pérez et al ., ).…”

“…Researchers have reached the consensus that surface freshwater systems (epilimnion) are ubiquitously dominated by bacterioplankton lineages represented by the phyla Actinobacteria, Proteobacteria and Bacteroidetes (Newton et al ., ). In addition, we have previously unveiled the vertical stratification of bacterioplankton communities in deep freshwater lakes, where the oxygenated hypolimnion – that is, the deep aerobic water layer below the thermocline, which generally constitutes a volumetrically significant part of deep temperate, oligo‐mesotrophic lakes – was dominated by specific lineages that are uncommon in the epilimnion, including members of Chloroflexi (Okazaki et al ., ; ), Planctomycetes, Nitrospira and Thaumarchaeota (Okazaki and Nakano, ; Okazaki et al ., ). These lineages are likely responsible for important biogeochemical processes in the oxygenated hypolimnion, such as remineralization or conversion of semi‐labile organic matter (Maki et al ., ; Thottathil et al ., ), nitrification (Small et al ., ; Alfreider et al ., ) and methane oxidation (Murase and Sugimoto, ).…”

Microdiversity and phylogeographic diversification of bacterioplankton in pelagic freshwater systems revealed through long-read amplicon sequencing

“…Lakes are physically disconnected ecosystems, and thus offer a good model for investigating the diversification and phylogeographic processes of microbes. Whereas 16S rRNA gene-based phylogenies have been used to characterize the cosmopolitan bacterioplankton lineages that are ubiquitously dominant in freshwater systems [36][37][38], analyses at finer phylogenetic resolution have been used to identify intra-lineage microdiversity and phylogeography. A global-scale investigation of microdiversity was conducted for the PnecC subcluster of the genus Polynucleobacter (Betaproteobacteria), a cosmopolitan freshwater bacterial group, using the ITS and glnA gene as markers, which showed distance-decay patterns and global-scale niche separation of subgroups adapted to different thermal conditions [15].…”

Comparing microbial composition and diversity in freshwater lakes between Greenland and the Tibetan Plateau

“…Cryptic microdiversification with almost identical 16S rRNA gene sequences within a ubiquitous freshwater lineage, for example, Limnohabitans and Polynucleobacter , has been reported (Jezbera et al 2011, 2013; Hahn et al 2015, 2016). Different sub‐populations were present among the lineages (e.g., acI–B1 and acI–A7) occurring in the entire water layer (Okazaki et al 2017). Coincidentally, a horizontal oligotype profile in Lake Michigan indicated oligotype differentiation between estuarine and pelagic sites (Newton and McLellan 2015).…”