The evolutionary origins of the bacterial lineages that populate the human gut are unknown. Here we show that multiple lineages of the predominant bacterial taxa in the gut arose via cospeciation with humans, chimpanzees, bonobos, and gorillas over the past 15 million years. Analyses of strain-level bacterial diversity within hominid gut microbiomes revealed that clades of Bacteroidaceae and Bifidobacteriaceae have been maintained exclusively within host lineages across hundreds of thousands of host generations. Divergence times of these cospeciating gut bacteria are congruent with those of hominids, indicating that nuclear, mitochondrial, and gut bacterial genomes diversified in concert during hominid evolution. This study identifies human gut bacteria descended from ancient symbionts that speciated simultaneously with humans and the African apes.
SummaryWhether or not bacterial species exist remains an unresolved issue of paramount theoretical as well as practical consequences. Here we review and synthesize the findings emerging from metagenomic surveys of natural microbial populations and argue that microbial communities are predominantly organized in genetically and ecologically discernible populations, which possess the attributes expected for species. These sequence-discrete populations represent a major foundation for beginning highresolution investigations on how populations are organized, interact, and evolve within communities. We also attempt to reconcile these findings with those of previous studies that reported indiscrete species and a genetic continuum within bacterial taxa and discuss the implications for the current bacterial species definition.
Lake Lanier is an important freshwater lake for the southeast United States, as it represents the main source of drinking water for the Atlanta metropolitan area and is popular for recreational activities. Temperate freshwater lakes such as Lake Lanier are underrepresented among the growing number of environmental metagenomic data sets, and little is known about how functional gene content in freshwater communities relates to that of other ecosystems. To better characterize the gene content and variability of this freshwater planktonic microbial community, we sequenced several samples obtained around a strong summer storm event and during the fall water mixing using a random whole-genome shotgun (WGS) approach. Comparative metagenomics revealed that the gene content was relatively stable over time and more related to that of another freshwater lake and the surface ocean than to soil. However, the phylogenetic diversity of Lake Lanier communities was distinct from that of soil and marine communities. We identified several important genomic adaptations that account for these findings, such as the use of potassium (as opposed to sodium) osmoregulators by freshwater organisms and differences in the community average genome size. We show that the lake community is predominantly composed of sequence-discrete populations and describe a simple method to assess community complexity based on population richness and evenness and to determine the sequencing effort required to cover diversity in a sample. This study provides the first comprehensive analysis of the genetic diversity and metabolic potential of a temperate planktonic freshwater community and advances approaches for comparative metagenomics.
High-throughput sequencing studies during the last decade have uncovered that bacterial genomes are very diverse and dynamic, resulting primarily from the frequent and promiscuous horizontal gene exchange that characterizes the bacterial domain of life. However, a robust understanding of the rates of genetic exchange for most bacterial species under natural conditions and the influence of the ecological settings on the rates remain elusive, severely limiting our view of the microbial world. Here, we analyzed the complete genomic sequences and expressed transcriptomes of several Shewanella baltica isolates recovered from different depths in the Baltic Sea and found that isolates from more similar depths had exchanged a larger fraction of their core and auxiliary genome, up to 20% of the total, compared with isolates from more different depths. The exchanged genes seem to be ecologically important and contribute to the successful adaptation of the isolates to the unique physicochemical conditions of the depth. Importantly, the latter genes were exchanged in very recent past, presumably as an effect of isolate's seasonal migration across the water column, and reflected sexual speciation within the same depth. Therefore, our findings reveal that genetic exchange in response to environmental settings may be surprisingly rapid, which has important broader impacts for understanding bacterial speciation and evolution and for modeling bacterial responses to human-induced environmental impacts.
The Louisiana Shelf in the Gulf of Mexico experiences recurrent bottom water hypoxia under summertime eutrophic conditions. The onset, maintenance, and breakdown of hypoxia are associated with dynamic microbial biogeochemical cycles. However, the distribution of microbial taxa and metabolisms across Shelf oxygen gradients remains under-characterized. We combined biogeochemical analyses of nitrogen (N) distributions and metabolic rates with metagenomic and metatranscriptomic analysis of summertime Shelf waters. Samples from an east-west transect during July 2012 revealed an inverse relationship between nitrite and oxygen concentrations, with concentrations exceeding 1 lmol L 21 at 50% oxygen saturation and reaching 4.6 lmol L 21 at the most oxygen-depleted sites. Historical data confirms that nitrite accumulation occurs frequently in this region both above and below the hypoxic threshold. Experimental incubations demonstrated a strong decoupling between the two steps of nitrification, with ammonia oxidation proceeding up to 30 times faster than nitrite oxidation under low oxygen. 16S rRNA gene, metagenome, and metatranscriptome sequencing revealed a diverse microbial community, stratified over shallow (< 10 m) depth gradients, with an enrichment of ammonia-oxidizing Thaumarchaeota genes and transcripts in deeper more oxygendepleted layers, and a comparatively low representation of sequences related to nitrite oxidation. A range of factors, including temperature and substrate availability, which may be linked indirectly to bottom water oxygen content, potentially drives decoupling of ammonia and nitrite oxidation on the Louisiana Shelf. Nitrite accumulation in hypoxic zones remains understudied and may have important effects on microbial nitrogen flux, algal dynamics, and production.
Spirochaetes is one of a few bacterial phyla that are characterized by a unifying diagnostic feature, namely, the helical morphology and motility conferred by axial periplasmic flagella. Their unique morphology and mode of propulsion also represent major pathogenicity factors of clinical spirochetes. Here we describe the genome sequences of two coccoid isolates of the recently described genus Sphaerochaeta which are members of the phylum Spirochaetes based on 16S rRNA gene and whole-genome phylogenies. Interestingly, the Sphaerochaeta genomes completely lack the motility and associated signal transduction genes present in all sequenced spirochete genomes. Additional analyses revealed that the lack of flagella is associated with a unique, nonrigid cell wall structure hallmarked by a lack of transpeptidase and transglycosylase genes, which is also unprecedented in spirochetes. The Sphaerochaeta genomes are highly enriched in fermentation and carbohydrate metabolism genes relative to other spirochetes, indicating a fermentative lifestyle. Remarkably, most of the enriched genes appear to have been acquired from nonspirochetes, particularly clostridia, in several massive horizontal gene transfer events (>40% of the total number of genes in each genome). Such a high level of direct interphylum genetic exchange is extremely rare among mesophilic organisms and has important implications for the assembly of the prokaryotic tree of life.
For both historical and technical reasons, 16S ribosomal RNA has been the most common molecular marker used to analyze the contents of microbial communities. However, its slow rate of evolution hinders the resolution of closely related bacteria—individual 16S-phylotypes, particularly when clustered at 97% sequence identity, conceal vast amounts of species- and strain-level variation. Protein-coding genes, which evolve more quickly, are useful for differentiating among more recently diverged lineages, but their application is complicated by difficulties in designing low-redundancy primers that amplify homologous regions from distantly related taxa. Given the now-common practice of multiplexing hundreds of samples, adopting new genes usually entails the synthesis of large sets of barcoded primers. To circumvent problems associated with use of protein-coding genes to survey microbial communities, we develop an approach—termed phyloTAGs—that offers an automatic solution for primer design and can be easily adapted to target different taxonomic groups and/or different protein-coding regions. We applied this method to analyze diversity within the gorilla gut microbiome and recovered hundreds of strains that went undetected after deep-sequencing of 16S rDNA amplicons. PhyloTAGs provides a powerful way to recover the fine-level diversity within microbial communities and to study stability and dynamics of bacterial populations.
Genome sequencing has revealed that horizontal gene transfer (HGT) is a major evolutionary process in bacteria. Although it is generally assumed that closely related organisms engage in genetic exchange more frequently than distantly related ones, the frequency of HGT among distantly related organisms and the effect of ecological relatedness on the frequency has not been rigorously assessed. Here, we devised a novel bioinformatic pipeline, which minimized the effect of overrepresentation of specific taxa in the available databases and other limitations of homology-based approaches by analyzing genomes in standardized triplets, to quantify gene exchange between bacterial genomes representing different phyla. Our analysis revealed the existence of networks of genetic exchange between organisms with overlapping ecological niches, with mesophilic anaerobic organisms showing the highest frequency of exchange and engaging in HGT twice as frequently as their aerobic counterparts. Examination of individual cases suggested that interphylum HGT is more pronounced than previously thought, affecting up to B16% of the total genes and B35% of the metabolic genes in some genomes (conservative estimation). In contrast, ribosomal and other universal protein-coding genes were subjected to HGT at least 150 times less frequently than genes encoding the most promiscuous metabolic functions (for example, various dehydrogenases and ABC transport systems), suggesting that the species tree based on the former genes may be reliable. These results indicated that the metabolic diversity of microbial communities within most habitats has been largely assembled from preexisting genetic diversity through HGT and that HGT accounts for the functional redundancy among phyla.
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