SUMMARY Freshwater bacteria are at the hub of biogeochemical cycles and control water quality in lakes. Despite this, little is known about the identity and ecology of functionally significant lake bacteria. Molecular studies have identified many abundant lake bacteria, but there is a large variation in the taxonomic or phylogenetic breadths among the methods used for this exploration. Because of this, an inconsistent and overlapping naming structure has developed for freshwater bacteria, creating a significant obstacle to identifying coherent ecological traits among these groups. A discourse that unites the field is sorely needed. Here we present a new freshwater lake phylogeny constructed from all published 16S rRNA gene sequences from lake epilimnia and propose a unifying vocabulary to discuss freshwater taxa. With this new vocabulary in place, we review the current information on the ecology, ecophysiology, and distribution of lake bacteria and highlight newly identified phylotypes. In the second part of our review, we conduct meta-analyses on the compiled data, identifying distribution patterns for bacterial phylotypes among biomes and across environmental gradients in lakes. We conclude by emphasizing the role that this review can play in providing a coherent framework for future studies.
Enhanced Biological Phosphorus Removal (EBPR) is not well understood at the metabolic level despite being one of the best-studied microbially-mediated industrial processes due to its ecological and economic relevance. Here we present a metagenomic analysis of two lab-scale EBPR sludges dominated by the uncultured bacterium, "Candidatus Accumulibacter phosphatis". This analysis sheds light on several controversies in EBPR metabolic models and provides hypotheses explaining the dominance of A. phosphatis in this habitat, its lifestyle outside EBPR and probable cultivation requirements.Comparison of the same species from different EBPR sludges highlights recent evolutionary dynamics in the A. phosphatis genome that could be linked to mechanisms for environmental adaptation. In spite of an apparent lack of phylogenetic overlap in the flanking communities of the two sludges studied, common functional themes were found, at least one of them complementary to the inferred metabolism of the dominant organism.The present study provides a much-needed blueprint for a systems-level understanding of EBPR and illustrates that metagenomics enables detailed, often novel, insights into even well-studied biological systems. 3Excessive inorganic phosphate (Pi) supply to freshwater negatively affects water quality and ecosystem balance through a process known as eutrophication 1 . Limitations on allowable Pi discharges from municipal and industrial sources via wastewater treatment have proven effective in reducing Pi levels in many waterways 2 . Increasingly stringent Pi limits for effluent wastewater are expected in the future and hence efficient and reliable Pi removal methods are required. Due to the massive quantity of wastewater treated daily (more than 120 billion liters in the US alone 3 ), any improvement in existing methods should have tangible economic and ecological consequences.Enhanced Biological Phosphorus Removal (EBPR) is a treatment process in which microorganisms remove Pi from wastewater by accumulating it inside their cells as polyphosphate. These polyphosphate-accumulating organisms (PAOs) are then allowed to settle in a separate tank (clarifier), leaving the effluent water largely Pi-depleted. EBPR is more economical in the long term 2 and has a lower environmental impact 4 than traditional (chemical) Pi removal 5 , but is prone to unpredictable failures due to loss or reduced activity of microbial populations responsible for Pi removal 6 . This is primarily because the design process is highly empirical due to an incomplete understanding of sludge microbial ecology. Environmental engineers and microbiologists have been studying EBPR since its introduction in municipal wastewater treatment plants over thirty years ago 5 with the goal of making it a more reliable industrial process. Typically, EBPR is studied in lab-scale sequencing batch reactors (SBRs) where the microbial community can be better monitored and perturbed, and PAOs can be enriched to much higher levels than in full scale systems 7 .For th...
Multiple models describe the formation and evolution of distinct microbial phylogenetic groups. These evolutionary models make different predictions regarding how adaptive alleles spread through populations and how genetic diversity is maintained. Processes predicted by competing evolutionary models, for example, genome-wide selective sweeps vs gene-specific sweeps, could be captured in natural populations using time-series metagenomics if the approach were applied over a sufficiently long time frame. Direct observations of either process would help resolve how distinct microbial groups evolve. Here, from a 9-year metagenomic study of a freshwater lake (2005–2013), we explore changes in single-nucleotide polymorphism (SNP) frequencies and patterns of gene gain and loss in 30 bacterial populations. SNP analyses revealed substantial genetic heterogeneity within these populations, although the degree of heterogeneity varied by >1000-fold among populations. SNP allele frequencies also changed dramatically over time within some populations. Interestingly, nearly all SNP variants were slowly purged over several years from one population of green sulfur bacteria, while at the same time multiple genes either swept through or were lost from this population. These patterns were consistent with a genome-wide selective sweep in progress, a process predicted by the ‘ecotype model' of speciation but not previously observed in nature. In contrast, other populations contained large, SNP-free genomic regions that appear to have swept independently through the populations prior to the study without purging diversity elsewhere in the genome. Evidence for both genome-wide and gene-specific sweeps suggests that different models of bacterial speciation may apply to different populations coexisting in the same environment.
We investigated the fine-scale population structure of the "Candidatus Accumulibacter" lineage in enhanced biological phosphorus removal (EBPR) systems using the polyphosphate kinase 1 gene (ppk1) as a genetic marker. We retrieved fragments of "Candidatus Accumulibacter" 16S rRNA and ppk1 genes from one laboratory-scale and several full-scale EBPR systems. Phylogenies reconstructed using 16S rRNA genes and ppk1 were largely congruent, with ppk1 granting higher phylogenetic resolution and clearer tree topology and thus serving as a better genetic marker than 16S rRNA for revealing population structure within the "Candidatus Accumulibacter" lineage. Sequences from at least five clades of "Candidatus Accumulibacter" were recovered by ppk1-targeted PCR, and subsequently, specific primer sets were designed to target the ppk1 gene for each clade. Quantitative real-time PCR (qPCR) assays using "Candidatus Accumulibacter"-specific 16S rRNA and "Candidatus Accumulibacter" clade-specific ppk1 primers were developed and conducted on three laboratoryscale and nine full-scale EBPR samples and two full-scale non-EBPR samples to determine the abundance of the total "Candidatus Accumulibacter" lineage and the relative distributions and abundances of the five "Candidatus Accumulibacter" clades. The qPCR-based estimation of the total "Candidatus Accumulibacter" fraction as a proportion of the bacterial community as measured using 16S rRNA genes was not significantly different from the estimation measured using ppk1, demonstrating the power of ppk1 as a genetic marker for detection of all currently defined "Candidatus Accumulibacter" clades. The relative distributions of "Candidatus Accumulibacter" clades varied among different EBPR systems and also temporally within a system. Our results suggest that the "Candidatus Accumulibacter" lineage is more diverse than previously realized and that different clades within the lineage are ecologically distinct.
Population dynamics are influenced by drivers acting from outside and from within an ecosystem. Extrinsic forces operating over broad spatial scales can impart synchronous behavior to separate populations, while internal, system-specific drivers often lead to idiosyncratic behavior. Here, we demonstrate synchrony in community-level dynamics among phytoplankton and bacteria in six north temperate humic lakes. The influence of regional meteorological factors explained much of the temporal variability in the phytoplankton community, and resulted in synchronous patterns of community change among lakes. Bacterial dynamics, in contrast, were driven by system-specific interactions with phytoplankton. Despite the importance of intrinsic factors for determining bacterial community composition and dynamics, we demonstrated that biological interactions transmitted the signal of the regional extrinsic drivers to the bacterial communities, ultimately resulting in synchronous community phenologies for bacterioplankton communities as well. This demonstrates how linkages between the components of a complex biological system can work to simplify the dynamics of the system and implies that it may be possible to predict the behavior of microbial communities responsible for important biogeochemical services in the landscape.
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