The cyanobacterium Prochlorococcus has divergent light-harvesting antennae and may have evolved in a low-oxygen ocean.

Marine picocyanobacteria of the genus Prochlorococcus are the most abundant photosynthetic organisms in the modern ocean, where they exert a profound influence on elemental cycling and energy flow. The use of transmembrane chlorophyll complexes instead of phycobilisomes as light-harvesting antennae is considered a defining attribute of Prochlorococcus Its ecology and evolution are understood in terms of light, temperature, and nutrients. Here, we report single-cell genomic information on previously uncharacterized phylogenetic lineages of this genus from nutrient-rich anoxic waters of the eastern tropical North and South Pacific Ocean. The most basal lineages exhibit optical and genotypic properties of phycobilisome-containing cyanobacteria, indicating that the characteristic light-harvesting antenna of the group is not an ancestral attribute. Additionally, we found that all the indigenous lineages analyzed encode genes for pigment biosynthesis under oxygen-limited conditions, a trait shared with other freshwater and coastal marine cyanobacteria. Our findings thus suggest that Prochlorococcus diverged from other cyanobacteria under low-oxygen conditions before transitioning from phycobilisomes to transmembrane chlorophyll complexes and may have contributed to the oxidation of the ancient ocean.

Redox traits characterize the organization of global microbial communities.

The structure of biological communities is conventionally described as profiles of taxonomic units, whose ecological functions are assumed to be known or, at least, predictable. In environmental microbiology, however, the functions of a majority of microorganisms are unknown and expected to be highly dynamic and collectively redundant, obscuring the link between taxonomic structure and ecosystem functioning. Although genetic trait-based approaches at the community level might overcome this problem, no obvious choice of gene categories can be identified as appropriate descriptive units in a general ecological context. We used 247 microbial metagenomes from 18 biomes to determine which set of genes better characterizes the differences among biomes on the global scale. We show that profiles of oxidoreductase genes support the highest biome differentiation compared with profiles of other categories of enzymes, general protein-coding genes, transporter genes, and taxonomic gene markers. Based on oxidoreductases' description of microbial communities, the role of energetics in differentiation and particular ecosystem function of different biomes become readily apparent. We also show that taxonomic diversity is decoupled from functional diversity, e.g., grasslands and rhizospheres were the most diverse biomes in oxidoreductases but not in taxonomy. Considering that microbes underpin biogeochemical processes and nutrient recycling through oxidoreductases, this functional diversity should be relevant for a better understanding of the stability and conservation of biomes. Consequently, this approach might help to quantify the impact of environmental stressors on microbial ecosystems in the context of the global-scale biome crisis that our planet currently faces.

Autotrophic carbon fixation pathways along the redox gradient in oxygen-depleted oceanic waters.

Anoxic marine zones (AMZs), also known as 'oxygen-deficient zones', contribute to the loss of fixed nitrogen from the ocean by anaerobic microbial processes. While these microbial processes associated with the nitrogen cycle have been extensively studied, those linked to the carbon cycle in AMZs have received much less attention, particularly the autotrophic carbon fixation - a crucial component of the carbon cycle. Using metagenomic and metatranscriptomic data from major AMZs, we report an explicit partitioning of the marker genes associated with different autotrophic carbon fixation pathways along the redox gradient (from oxic to anoxic conditions) present in the water column of AMZs. Sequences related to the Calvin-Benson-Bassham cycle were found along the entire gradient, while those related to the reductive Acetyl-CoA pathway were restricted to suboxic and anoxic waters. Sequences putatively associated with the 3-hydroxypropionate/4-hydroxybutyrate cycle dominated in the upper and lower oxyclines. Genes related to the reductive tricarboxylic acid cycle were represented from dysoxic to anoxic waters. The taxonomic affiliation of the sequences is consistent with the presence of microorganisms involved in crucial steps of biogeochemical cycles in AMZs, such as the gamma-proteobacteria sulfur oxidisers, the anammox bacteria Candidatus Scalindua and the thaumarcheota ammonia oxidisers of the Marine Group I.

Bosque: integrated phylogenetic analysis software.

UNLABELLED: Phylogenetic analyses today involve dealing with computer files in different formats and often several computer programs. Although some widely used applications have integrated important functionalities for such analyses, they still work with local resources only: input/output files (users have to manage them) and local computing (users have sometimes to leave their programs, on their desktop computers, running for extended periods of time). To address these problems we have developed 'Bosque', a multi-platform client-server software that performs standard phylogenetic tasks either locally or remotely on servers, and integrates the results on a local relational database. Bosque performs sequence alignments and graphical visualization and editing of trees, thus providing a powerful environment that integrates all the steps of phylogenetic analyses. AVAILABILITY: http://bosque.udec.cl

Distinctive Archaeal Composition of an Artisanal Crystallizer Pond and Functional Insights Into Salt-Saturated Hypersaline Environment Adaptation.

Hypersaline environments represent some of the most challenging settings for life on Earth. Extremely halophilic microorganisms have been selected to colonize and thrive in these extreme environments by virtue of a broad spectrum of adaptations to counter high salinity and osmotic stress. Although there is substantial data on microbial taxonomic diversity in these challenging ecosystems and their primary osmoadaptation mechanisms, less is known about how hypersaline environments shape the genomes of microbial inhabitants at the functional level. In this study, we analyzed the microbial communities in five ponds along the discontinuous salinity gradient from brackish to salt-saturated environments and sequenced the metagenome of the salt (halite) precipitation pond in the artisanal Cáhuil Solar Saltern system. We combined field measurements with spectrophotometric pigment analysis and flow cytometry to characterize the microbial ecology of the pond ecosystems, including primary producers and applied metagenomic sequencing for analysis of archaeal and bacterial taxonomic diversity of the salt crystallizer harvest pond. Comparative metagenomic analysis of the Cáhuil salt crystallizer pond against microbial communities from other salt-saturated aquatic environments revealed a dominance of the archaeal genus Halorubrum and showed an unexpectedly low abundance of Haloquadratum in the Cáhuil system. Functional comparison of 26 hypersaline microbial metagenomes revealed a high proportion of sequences associated with nucleotide excision repair, helicases, replication and restriction-methylation systems in all of them. Moreover, we found distinctive functional signatures between the microbial communities from salt-saturated (>30% [w/v] total salinity) compared to sub-saturated hypersaline environments mainly due to a higher representation of sequences related to replication, recombination and DNA repair in the former. The current study expands our understanding of the diversity and distribution of halophilic microbial populations inhabiting salt-saturated habitats and the functional attributes that sustain them.

Genomic potential for nitrogen assimilation in uncultivated members of Prochlorococcus from an anoxic marine zone.

Cyanobacteria of the genus Prochlorococcus are the most abundant photosynthetic marine organisms and key factors in the global carbon cycle. The understanding of their distribution and ecological importance in oligotrophic tropical and subtropical waters, and their differentiation into distinct ecotypes, is based on genetic and physiological information from several isolates. Currently, all available Prochlorococcus genomes show their incapacity for nitrate utilization. However, environmental sequence data suggest that some uncultivated lineages may have acquired this capacity. Here we report that uncultivated low-light-adapted Prochlorococcus from the nutrient-rich, low-light, anoxic marine zone (AMZ) of the eastern tropical South Pacific have the genetic potential for nitrate uptake and assimilation. All genes involved in this trait were found syntenic with those present in marine Synechococcus. Genomic and phylogenetic analyses also suggest that these genes have not been aquired recently, but perhaps were retained from a common ancestor, highlighting the basal characteristics of the AMZ lineages within Prochlorococcus.