Conserved synteny at the protein family level reveals genes underlying Shewanella species’ cold tolerance and predicts their novel phenotypes

© The Authors 2009. This article is distributed under the terms of the Creative Commons Attribution Noncommercial License. The definitive version was published in Functional & Integrative Genomics 10 (2010): 97-110, doi:10.1007/s10142-009-0142-y.Bacteria of the genus Shewanella can thrive in different environments and demonstrate significant variability in their metabolic and ecophysiological capabilities including cold and salt tolerance. Genomic characteristics underlying this variability across species are largely unknown. In this study, we address the problem by a comparison of the physiological, metabolic, and genomic characteristics of 19 sequenced Shewanella species. We have employed two novel approaches based on association of a phenotypic trait with the number of the trait-specific protein families (Pfam domains) and on the conservation of synteny (order in the genome) of the trait-related genes. Our first approach is top-down and involves experimental evaluation and quantification of the species’ cold tolerance followed by identification of the correlated Pfam domains and genes with a conserved synteny. The second, a bottom-up approach, predicts novel phenotypes of the species by calculating profiles of each Pfam domain among their genomes and following pair-wise correlation of the profiles and their network clustering. Using the first approach, we find a link between cold and salt tolerance of the species and the presence in the genome of a Na+/H+ antiporter gene cluster. Other cold-tolerance-related genes include peptidases, chemotaxis sensory transducer proteins, a cysteine exporter, and helicases. Using the bottom-up approach, we found several novel phenotypes in the newly sequenced Shewanella species, including degradation of aromatic compounds by an aerobic hybrid pathway in Shewanella woodyi, degradation of ethanolamine by Shewanella benthica, and propanediol degradation by Shewanella putrefaciens CN32 and Shewanella sp. W3-18-1.This research was supported by the U.S. Department of Energy (DOE) Office of Biological and Environmental Research under the Genomics: GTL Program via the Shewanella Federation consortium

Widespread adenine N6-methylation of active genes in fungi.

N6-methyldeoxyadenine (6mA) is a noncanonical DNA base modification present at low levels in plant and animal genomes, but its prevalence and association with genome function in other eukaryotic lineages remains poorly understood. Here we report that abundant 6mA is associated with transcriptionally active genes in early-diverging fungal lineages. Using single-molecule long-read sequencing of 16 diverse fungal genomes, we observed that up to 2.8% of all adenines were methylated in early-diverging fungi, far exceeding levels observed in other eukaryotes and more derived fungi. 6mA occurred symmetrically at ApT dinucleotides and was concentrated in dense methylated adenine clusters surrounding the transcriptional start sites of expressed genes; its distribution was inversely correlated with that of 5-methylcytosine. Our results show a striking contrast in the genomic distributions of 6mA and 5-methylcytosine and reinforce a distinct role for 6mA as a gene-expression-associated epigenomic mark in eukaryotes

Methanogens and Methanogenesis in Hypersaline Environments

Methanogenesis is controlled by redox potential and permanency of anaerobic conditions; and in hypersaline environments, the high concentration of terminal electron acceptors, particularly sulfate, is an important controlling factor. This is because sulfate-reducing microbes, compared with methanogens, have a greater affinity for, and energy yield from, competitive substrates like hydrogen and acetate. However, hypersalinity is not an obstacle to methylotrophic methanogenesis; in many cases hypersaline environments have high concentrations of noncompetitive substrates like methylamines, which derive from compatible solutes such as glycine betaine that is synthesized by many microbes inhabiting hypersaline environments. Also, depletion of sulfate, as may occur in deeper sediments, allows increased methanogenesis. On the other hand, increasing salinity requires methanogens to synthesize or take up more compatible solutes at a significant energetic cost. Acetoclastic and hydrogenotrophic methanogens, with their lower energetic yields, are therefore more susceptible than methylotrophic methanogens, which further explains the predominance of methylotrophic methanogens like Methanohalophilus and Methanohalobium spp. in hypersaline environments. There are often deviations from the picture outlined above, which are sometimes difficult to explain. Identifying the role of uncultivated Euryarchaeota in hypersaline environments, elucidating the effects of different ions (which have differential stress effects and potential as electron acceptors), and understanding the effects of salinity on all microbes involved in methane cycling will help us to understand and predict methane production in hypersaline environments. A good demonstration of this is a recent discovery of extremely haloalkaliphilic methanogens living in hypersaline lakes, which utilize the methyl-reducing pathway and form a novel class “Methanonatronarchaeia” in the Euryarchaeota