Multiple adaptations to polar and alpine environments within cyanobacteria:a phylogenomic and Bayesian approach

Cyanobacteria are major primary producers in the polar and alpine regions contributing significantly to nitrogen and carbon cycles in the cryosphere. Recent advancements in environmental sequencing techniques have revealed great molecular diversity of microorganisms in cold environments. However, there are no comprehensive phylogenetic analyses including the entire known diversity of cyanobacteria from these extreme environments. We present here a global phylogenetic analysis of cyanobacteria including an extensive dataset comprised of available SSU rRNA gene sequences of cyanobacteria from polar and high altitude environments. Furthermore, we used a large-scale multi-gene (135 proteins and two ribosomal RNAs) genome constraint including 57 cyanobacterial genomes. Our analyses produced the first phylogeny of cold cyanobacteria exhibiting robust deep branching relationships implementing a phylogenomic approach. We recovered several clades common to Arctic, Antarctic and alpine sites suggesting that the traits necessary for survival in the cold have been acquired by a range of different mechanisms in all major cyanobacteria lineages. Bayesian ancestral state reconstruction revealed that twenty clades each have common ancestors with high probabilities of being capable of surviving in cold environments

Insights Into the Evolution of Picocyanobacteria and Phycoerythrin Genes (mpeBA and cpeBA)

Marine picocyanobacteria, Prochlorococcus and Synechococcus, substantially contribute to marine primary production and have been the subject of extensive ecological and genomic studies. Little is known about their close relatives from freshwater and non-marine environments. Phylogenomic analyses (using 136 proteins) provide strong support for the monophyly of a clade of non-marine picocyanobacteria consisting of Cyanobium, Synechococcus and marine Sub-cluster 5.2; this clade itself is sister to marine Synechococcus and Prochlorococcus. The most basal lineage within the Syn/Pro clade, Sub-Cluster 5.3, includes marine and freshwater strains. Relaxed molecular clock (SSU, LSU) analyses show that while ancestors of the Syn/Pro clade date as far back as the end of the Pre-Cambrian, modern crown groups evolved during the Carboniferous and Triassic. Comparative genomic analyses reveal novel gene cluster arrangements involved in phycobilisome (PBS) metabolism in freshwater strains. Whilst PBS genes in marine Synechococcus are mostly found in one type of phycoerythrin (PE) rich gene cluster (Type III), strains from non-marine habitats, so far, appear to be more diverse both in terms of pigment content and gene arrangement, likely reflecting a wider range of habitats. Our phylogenetic analyses show that the PE genes (mpeBA) evolved via a duplication of the cpeBA genes in an ancestor of the marine and non-marine picocyanobacteria and of the symbiotic strains Synechococcus spongiarum. A ‘primitive’ Type III-like ancestor containing cpeBA and mpeBA had thus evolved prior to the divergence of the Syn/Pro clade and S. spongiarum. During the diversification of Synechococcus lineages, losses of mpeBA genes may explain the emergence of pigment cluster Types I, II, IIB, and III in both marine and non-marine habitats, with few lateral gene transfer events in specific taxa

Algae drive enhanced darkening of bare ice on the Greenland ice sheet

Surface ablation of the Greenland ice sheet is amplified by surface darkening caused by light-absorbing impurities such as mineral dust, black carbon, and pigmented microbial cells. We present the first quantitative assessment of the microbial contribution to the ice sheet surface darkening, based on field measurements of surface reflectance and concentrations of light-absorbing impurities, including pigmented algae, during the 2014 melt season in the southwestern part of the ice sheet. The impact of algae on bare ice darkening in the study area was greater than that of non-algal impurities and yielded a net albedo reduction of 0.038 ± 0.0035 for each algal population doubling. We argue that algal growth is a crucial control of bare ice darkening, and incorporating the algal darkening effect will improve mass balance and sea level projections of the Greenland ice sheet and ice masses elsewhere

Total predicted protein associated Fe.

<p>Total protein derived Fe concentration for each of the four experimental treatments (T1+, T2+, T1- and T2-) expressed as fmol Fe ug^-1 total protein. Fe concentration is subdivided into the major Fe containing complexes: Nitrogenase, cytochrome <i>b</i>₆<i>f</i>, PSII, PSI and other.</p

Average concentration of select multi-subunit protein complexes.

<p>Average concentration ± standard error (fmol.μg^-1 total protein) for select multi-subunit protein complexes observed across each of the 4 samples. Bracketed and in italic font are the complex:PSII ratios.</p><p>Average concentration of select multi-subunit protein complexes.</p

Observed abundance and fold change of selected proteins.

<p>All the specifically mentioned proteins alongside their abundances (fmol μg^-1). Fold changes are shown as sparklines (blue = more abundant during Fe-deplete conditions, red = more abundant during Fe-replete conditions) and statistical significance of change is denoted with an asterisk. The reporting in previous studies is listed in the final column.</p

Linear electron flow schematic during high and low Fe conditions.

<p>Simplified schematic demonstrating the linear electron transport pathway during both high Fe (A, T1+) and low Fe (B, T1-) conditions. Protein complexes are shown as circles with their diameter indicative of observed complex concentration. Circles are coloured so as to show the predicted Fe concentration of that protein complex. Abbreviations include–PSII–photosystem II, Cyt b₆f –Cytochrome b₆f, PSI–photosystem I, Pc–plastocyanin, IsiA–iron stress induced protein A, Fv–Flavodoxin, FNR–Ferredoxin-NADP reductase, Rbc–RuBisCO, Nif–nitrogenase, ATP synthase–adenosine triphosphate synthase.</p