Glaciers and ice sheets, like other biomes, occupy a significant area of the planet and harbour biological communities with distinct interactions and feedbacks with their physical and chemical environment. In the case of the glacial biome, the biological processes are dominated almost exclusively by microbial communities. Habitats on glaciers and ice sheets with enough liquid water to sustain microbial activity include snow, surface ice, cryoconite holes, englacial systems and the interface between ice and overridden rock/soil. There is a remarkable similarity between the different specific glacial habitats across glaciers and ice sheets worldwide, particularly regarding their main primary producers and ecosystem engineers. At the surface, cyanobacteria dominate the carbon production in aquatic/sediment systems such as cryoconite holes, while eukaryotic Zygnematales and Chlamydomonadales dominate ice surfaces and snow dynamics, respectively. Microbially driven chemolithotrophic processes associated with sulphur and iron cycle and C transformations in subglacial ecosystems provide the basis for chemical transformations at the rock interface under the ice that underpin an important mechanism for the delivery of nutrients to downstream ecosystems. In this review, we focus on the main ecosystem engineers of glaciers and ice sheets and how they interact with their chemical and physical environment. We then discuss the implications of this microbial activity on the icy microbiome to the biogeochemistry of downstream ecosystems.
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 nonalgal 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.
BackgroundCyanobacteria are major primary producers in extreme cold ecosystems. Many lineages of cyanobacteria thrive in these harsh environments, but it is not fully understood how they survive in these conditions and whether they have evolved specific mechanisms of cold adaptation. Phormidesmis priestleyi is a cyanobacterium found throughout the cold biosphere (Arctic, Antarctic and alpine habitats). Genome sequencing of P. priestleyi BC1401, an isolate from a cryoconite hole on the Greenland Ice Sheet, has allowed for the examination of genes involved in cold shock response and production of extracellular polymeric substances (EPS). EPSs likely enable cyanobacteria to buffer the effects of extreme cold and by identifying mechanisms for EPS production in P. priestleyi BC1401 this study lays the way for investigating transcription and regulation of EPS production in an ecologically important cold tolerant cyanobacterium.ResultsWe sequenced the draft genome of P. priestleyi BC1401 and implemented a new de Bruijn graph visualisation approach combined with BLAST analysis to separate cyanobacterial contigs from a simple metagenome generated from non-axenic cultures. Comparison of known cold adaptation genes in P. priestleyi BC1401 with three relatives from other environments revealed no clear differences between lineages. Genes involved in EPS biosynthesis were identified from the Wzy- and ABC-dependent pathways. The numbers of genes involved in cell wall and membrane biogenesis in P. priestleyi BC1401 were typical relative to the genome size. A gene cluster implicated in biofilm formation was found homologous to the Wps system, although the intracellular signalling pathways by which this could be regulated remain unclear.ConclusionsResults show that the genomic characteristics and complement of known cold shock genes in P. priestleyi BC1401 are comparable to related lineages from a wide variety of habitats, although as yet uncharacterised cold shock genes in this organism may still exist. EPS production by P. priestleyi BC1401 likely contributes to its ability to survive efficiently in cold environments, yet this mechanism is widely distributed throughout the cyanobacterial phylum. Discovering how these EPS related mechanisms are regulated may help explain why P. priestleyi BC1401 is so successful in cold environments where related lineages are not.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2846-4) contains supplementary material, which is available to authorized users.
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.
Citation:Chrismas NAM, Anesio AM and Sánchez-Baracaldo P (2015) Multiple adaptations to polar and alpine environments within cyanobacteria : a phylogenomic and Bayesian approach. Front. Microbiol. 6:1070. doi: 10.3389/fmicb.2015.01070 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 small subunit (SSU) rRNA gene sequences of cyanobacteria from polar and high altitude environments. Furthermore, we used a large-scale multi-gene (135 proteins and 2 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 20 clades each have common ancestors with high probabilities of being capable of surviving in cold environments.
Trichodesmium is a biogeochemically important marine cyanobacterium, responsible for a significant proportion of the annual ‘new’ nitrogen introduced into the global ocean. These non-heterocystous filamentous diazotrophs employ a potentially unique strategy of near-concurrent nitrogen fixation and oxygenic photosynthesis, potentially burdening Trichodesmium with a particularly high iron requirement due to the iron-binding proteins involved in these processes. Iron availability may therefore have a significant influence on the biogeography of Trichodesmium. Previous investigations of molecular responses to iron stress in this keystone marine microbe have largely been targeted. Here a holistic approach was taken using a label-free quantitative proteomics technique (MSE) to reveal a sophisticated multi-faceted proteomic response of Trichodesmium erythraeum IMS101 to iron stress. Increased abundances of proteins known to be involved in acclimation to iron stress and proteins known or predicted to be involved in iron uptake were observed, alongside decreases in the abundances of iron-binding proteins involved in photosynthesis and nitrogen fixation. Preferential loss of proteins with a high iron content contributed to overall reductions of 55–60% in estimated proteomic iron requirements. Changes in the abundances of iron-binding proteins also suggested the potential importance of alternate photosynthetic pathways as Trichodesmium reallocates the limiting resource under iron stress. Trichodesmium therefore displays a significant and integrated proteomic response to iron availability that likely contributes to the ecological success of this species in the ocean.
Key to the ecological prominence of fungi is their distinctive cell biology, our understanding of which has been principally based on dikaryan hyphal and yeast forms. The early-diverging Chytridiomycota (chytrids) are ecologically important and a significant component of fungal diversity, yet their cell biology remains poorly understood. Unlike dikaryan hyphae, chytrids typically attach to substrates and feed osmotrophically via anucleate rhizoids. The evolution of fungal hyphae appears to have occurred from rhizoid-bearing lineages and it has been hypothesized that a rhizoid-like structure was the precursor to multicellular hyphae. Here, we show in a unicellular chytrid, Rhizoclosmatium globosum , that rhizoid development exhibits striking similarities with dikaryan hyphae and is adaptive to resource availability. Rhizoid morphogenesis exhibits analogous patterns to hyphal growth and is controlled by β-glucan-dependent cell wall synthesis and actin polymerization. Chytrid rhizoids growing from individual cells also demonstrate adaptive morphological plasticity in response to resource availability, developing a searching phenotype when carbon starved and spatial differentiation when interacting with particulate organic matter. We demonstrate that the adaptive cell biology and associated developmental plasticity considered characteristic of hyphal fungi are shared more widely across the Kingdom Fungi and therefore could be conserved from their most recent common ancestor.
BackgroundMany cyanobacteria are capable of fixing atmospheric nitrogen, playing a crucial role in biogeochemical cycling. Little is known about freshwater unicellular cyanobacteria Synechococcus spp. at the genomic level, despite being recognised of considerable ecological importance in aquatic ecosystems. So far, it has not been shown whether these unicellular picocyanobacteria have the potential for nitrogen fixation. Here, we present the draft-genome of the new pink-pigmented Synechococcus-like strain Vulcanococcus limneticus.sp. nov., isolated from the volcanic Lake Albano (Central Italy).ResultsThe novel species Vulcanococcus limneticus sp. nov. falls inside the sub-cluster 5.2, close to the estuarine/marine strains in a maximum-likelihood phylogenetic tree generated with 259 marker genes with representatives from marine, brackish, euryhaline and freshwater habitats. V.limneticus sp. nov. possesses a complete nitrogenase and nif operon. In an experimental setup under nitrogen limiting and non-limiting conditions, growth was observed in both cases. However, the nitrogenase genes (nifHDK) were not transcribed, i.e., V.limneticus sp. nov. did not fix nitrogen, but instead degraded the phycobilisomes to produce sufficient amounts of ammonia. Moreover, the strain encoded many other pathways to incorporate ammonia, nitrate and sulphate, which are energetically less expensive for the cell than fixing nitrogen. The association of the nif operon to a genomic island, the relatively high amount of mobile genetic elements (52 transposases) and the lower observed GC content of V.limneticus sp. nov. nif operon (60.54%) compared to the average of the strain (68.35%) support the theory that this planktonic strain may have obtained, at some point of its evolution, the nif operon by horizontal gene transfer (HGT) from a filamentous or heterocystous cyanobacterium.ConclusionsIn this study, we describe the novel species Vulcanococcus limneticus sp. nov., which possesses a complete nif operon for nitrogen fixation. The finding that in our experimental conditions V.limneticus sp. nov. did not express the nifHDK genes led us to reconsider the actual ecological meaning of these accessory genes located in genomic island that have possibly been acquired via HGT.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4648-3) contains supplementary material, which is available to authorized users.
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