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      Genome and metabolic network of “ Candidatus Phaeomarinobacter ectocarpi” Ec32, a new candidate genus of Alphaproteobacteria frequently associated with brown algae

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          Abstract

          Rhizobiales and related orders of Alphaproteobacteria comprise several genera of nodule-inducing symbiotic bacteria associated with plant roots. Here we describe the genome and the metabolic network of “ Candidatus Phaeomarinobacter ectocarpi” Ec32, a member of a new candidate genus closely related to Rhizobiales and found in association with cultures of the filamentous brown algal model Ectocarpus. The “ Ca. P. ectocarpi” genome encodes numerous metabolic pathways that may be relevant for this bacterium to interact with algae. Notably, it possesses a large set of glycoside hydrolases and transporters, which may serve to process and assimilate algal metabolites. It also harbors several proteins likely to be involved in the synthesis of algal hormones such as auxins and cytokinins, as well as the vitamins pyridoxine, biotin, and thiamine. As of today, “ Ca. P. ectocarpi” has not been successfully cultured, and identical 16S rDNA sequences have been found exclusively associated with Ectocarpus. However, related sequences (≥97% identity) have also been detected free-living and in a Fucus vesiculosus microbiome barcoding project, indicating that the candidate genus “ Phaeomarinobacter” may comprise several species, which may colonize different niches.

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          Most cited references55

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          Estimating the timing of early eukaryotic diversification with multigene molecular clocks.

          Although macroscopic plants, animals, and fungi are the most familiar eukaryotes, the bulk of eukaryotic diversity is microbial. Elucidating the timing of diversification among the more than 70 lineages is key to understanding the evolution of eukaryotes. Here, we use taxon-rich multigene data combined with diverse fossils and a relaxed molecular clock framework to estimate the timing of the last common ancestor of extant eukaryotes and the divergence of major clades. Overall, these analyses suggest that the last common ancestor lived between 1866 and 1679 Ma, consistent with the earliest microfossils interpreted with confidence as eukaryotic. During this interval, the Earth's surface differed markedly from today; for example, the oceans were incompletely ventilated, with ferruginous and, after about 1800 Ma, sulfidic water masses commonly lying beneath moderately oxygenated surface waters. Our time estimates also indicate that the major clades of eukaryotes diverged before 1000 Ma, with most or all probably diverging before 1200 Ma. Fossils, however, suggest that diversity within major extant clades expanded later, beginning about 800 Ma, when the oceans began their transition to a more modern chemical state. In combination, paleontological and molecular approaches indicate that long stems preceded diversification in the major eukaryotic lineages.
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            The Ectocarpus genome and the independent evolution of multicellularity in brown algae.

            Brown algae (Phaeophyceae) are complex photosynthetic organisms with a very different evolutionary history to green plants, to which they are only distantly related. These seaweeds are the dominant species in rocky coastal ecosystems and they exhibit many interesting adaptations to these, often harsh, environments. Brown algae are also one of only a small number of eukaryotic lineages that have evolved complex multicellularity (Fig. 1). We report the 214 million base pair (Mbp) genome sequence of the filamentous seaweed Ectocarpus siliculosus (Dillwyn) Lyngbye, a model organism for brown algae, closely related to the kelps (Fig. 1). Genome features such as the presence of an extended set of light-harvesting and pigment biosynthesis genes and new metabolic processes such as halide metabolism help explain the ability of this organism to cope with the highly variable tidal environment. The evolution of multicellularity in this lineage is correlated with the presence of a rich array of signal transduction genes. Of particular interest is the presence of a family of receptor kinases, as the independent evolution of related molecules has been linked with the emergence of multicellularity in both the animal and green plant lineages. The Ectocarpus genome sequence represents an important step towards developing this organism as a model species, providing the possibility to combine genomic and genetic approaches to explore these and other aspects of brown algal biology further.
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              Cultivating the uncultured.

              The recent application of molecular phylogeny to environmental samples has resulted in the discovery of an abundance of unique and previously unrecognized microorganisms. The vast majority of this microbial diversity has proved refractory to cultivation. Here, we describe a universal method that provides access to this immense reservoir of untapped microbial diversity. This technique combines encapsulation of cells in gel microdroplets for massively parallel microbial cultivation under low nutrient flux conditions, followed by flow cytometry to detect microdroplets containing microcolonies. The ability to grow and study previously uncultured organisms in pure culture will enhance our understanding of microbial physiology and metabolic adaptation and will provide new sources of microbial metabolites. We show that this technology can be applied to samples from several different environments, including seawater and soil.
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                Author and article information

                Contributors
                Journal
                Front Genet
                Front Genet
                Front. Genet.
                Frontiers in Genetics
                Frontiers Media S.A.
                1664-8021
                29 May 2014
                25 July 2014
                2014
                : 5
                : 241
                Affiliations
                [1] 1Sorbonne Universités, UPMC Univ. Paris 06, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff Roscoff, France
                [2] 2CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff Roscoff, France
                [3] 3CNRS, IRISA UMR 6074 Rennes, France
                [4] 4IRISA UMR 6074, Université de Rennes 1 Rennes, France
                [5] 5INRIA, Centre Rennes-Bretagne-Atlantique, Projet Dyliss Rennes, France
                [6] 6Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile Santiago, Chile
                Author notes

                Edited by: Josselin Noirel, University of Sheffield, UK

                Reviewed by: Jags Pandhal, University of Sheffield, UK; Matthew Alexander Fuszard, University of St Andrews, UK

                *Correspondence: Simon M. Dittami and Thierry Tonon, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, Place Georges Teissier, CS 90074, F-29688 Roscoff, France e-mail: simon.dittami@ 123456sb-roscoff.fr ; tonon@ 123456sb-roscoff.fr

                This article was submitted to Systems Biology, a section of the journal Frontiers in Genetics.

                Article
                10.3389/fgene.2014.00241
                4110880
                25120558
                9bdd9c81-0e33-4a36-b481-9dbf8f21f1ed
                Copyright © 2014 Dittami, Barbeyron, Boyen, Cambefort, Collet, Delage, Gobet, Groisillier, Leblanc, Michel, Scornet, Siegel, Tapia and Tonon.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 30 April 2014
                : 07 July 2014
                Page count
                Figures: 4, Tables: 2, Equations: 0, References: 72, Pages: 13, Words: 10352
                Categories
                Physiology
                Original Research Article

                Genetics
                holobiont,algal-bacterial interactions,genome sequencing,metabolic network,symbiosis,transporters,vitamins,phytohormones

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