The Phototrophic Consortium “Chlorochromatium aggregatum” – A Model for Bacterial Heterologous Multicellularity

Overmann, Jörg

doi:10.1007/978-1-4419-1528-3_2

Cited by 25 publications

(16 citation statements)

References 26 publications

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“…SOUL3 is localized to the plastid eyespot of C. reinhardtii (21) and, when knocked-out, the eyespot is reduced in size and its location is altered, negatively impacting phototaxis (21). AtHBP5 and SOUL3, which facilitate a coordinated response to light of the photosynthetic cell, produce an analogous phenotype to the communal phototropism of the wellknown prokaryotic consortium Chlorochromatium aggregatum (22). In the latter case, cross-talk between photosynthetic epibiontic bacteria is transferred to a central motile, brown bacterium, thereby moving the collective to a location where epibionts can most efficiently perform photosynthesis (22).…”

Section: Significancementioning

confidence: 99%

Protein networks identify novel symbiogenetic genes resulting from plastid endosymbiosis

Méheust

Zelzion

Bhattacharya

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The integration of foreign genetic information is central to the evolution of eukaryotes, as has been demonstrated for the origin of the Calvin cycle and of the heme and carotenoid biosynthesis pathways in algae and plants. For photosynthetic lineages, this coordination involved three genomes of divergent phylogenetic origins (the nucleus, plastid, and mitochondrion). Major hurdles overcome by the ancestor of these lineages were harnessing the oxygen-evolving organelle, optimizing the use of light, and stabilizing the partnership between the plastid endosymbiont and host through retargeting of proteins to the nascent organelle. Here we used protein similarity networks that can disentangle reticulate gene histories to explore how these significant challenges were met. We discovered a previously hidden component of algal and plant nuclear genomes that originated from the plastid endosymbiont: symbiogenetic genes (S genes). These composite proteins, exclusive to photosynthetic eukaryotes, encode a cyanobacteriumderived domain fused to one of cyanobacterial or another prokaryotic origin and have emerged multiple, independent times during evolution. Transcriptome data demonstrate the existence and expression of S genes across a wide swath of algae and plants, and functional data indicate their involvement in tolerance to oxidative stress, phototropism, and adaptation to nitrogen limitation. Our research demonstrates the "recycling" of genetic information by photosynthetic eukaryotes to generate novel composite genes, many of which function in plastid maintenance.gene fusion | endosymbiosis | photosynthesis | eukaryote evolution | novel gene origin T he genomes of the proteobacterium-derived mitochondrion and the cyanobacterium-derived plastid have undergone significant genome reduction due to outright gene loss or transfer to the nuclear genome (1, 2). Organelle gene loss by transfer to the nucleus is known as endosymbiotic gene transfer [EGT (a special form of horizontal gene transfer; HGT)] and has resulted in chimeric host nuclear genomes with, in the case of plastids, from ca. 200 to several thousand intact endosymbiont genes being relocated (3) (Fig. 1A). Plastid EGT has a long evolutionary history, extending back over a billion years in the case of primary plastid origin in the Archaeplastida (glaucophytes, red and green algae, and their sister group, plants) and several hundred million years for secondary plastids in groups such as diatoms, haptophytes, and dinoflagellates (4). A common fate for many nuclear-encoded organelle-derived proteins is to be targeted back to the compartment of origin via channels [i.e., translocons at the outer-and inner-envelope membrane of plastids and mitochondria (Toc/Tic and Tom/Tim, respectively)] to carry out organelle functions (5). Identification of EGT candidates generally relies on phylogenetic methods that use simultaneous alignment of colinear proteins sharing significant sequence similarity over all, or most, of their lengths to reconstruct the tree and its constituent ...

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Section: Significancementioning

confidence: 99%

Protein networks identify novel symbiogenetic genes resulting from plastid endosymbiosis

Méheust

Zelzion

Bhattacharya

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…chlorocromatii CaD3 changes between symbiosis and free-living states. Wenter et al (2010) and Overmann (2010) postulate that this bacterium in symbiosis is in a condition of low nitrogen availability, where the assimilation of ammonia becomes fundamental. The shift in the metabolic networks observed in our analysis supports this hypothesis.…”

Section: Is Nitrogen Assimilated Via Aladh In Free-living State?mentioning

confidence: 99%

Metabolic analysis of Chlorobium chlorochromatii CaD3 reveals clues of the symbiosis in ‘Chlorochromatium aggregatum’

et al. 2013

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A symbiotic association occurs in 'Chlorochromatium aggregatum', a phototrophic consortium integrated by two species of phylogenetically distant bacteria composed by the green-sulfur Chlorobium chlorochromatii CaD3 epibiont that surrounds a central b-proteobacterium. The nonmotile chlorobia can perform nitrogen and carbon fixation, using sulfide as electron donors for anoxygenic photosynthesis. The consortium can move due to the flagella present in the central b-protobacterium. Although Chl. chlorochromatii CaD3 is never found as free-living bacteria in nature, previous transcriptomic and proteomic studies have revealed that there are differential transcription patterns between the symbiotic and free-living status of Chl. chlorocromatii CaD3 when grown in laboratory conditions. The differences occur mainly in genes encoding the enzymatic reactions involved in nitrogen and amino acid metabolism. We performed a metabolic reconstruction of Chl. chlorochromatii CaD3 and an in silico analysis of its amino acid metabolism using an elementary flux modes approach (EFM). Our study suggests that in symbiosis, Chl. chlorochromatii CaD3 is under limited nitrogen conditions where the GS/GOGAT (glutamine synthetase/glutamate synthetase) pathway is actively assimilating ammonia obtained via N 2 fixation. In contrast, when free-living, Chl. chlorochromatii CaD3 is in a condition of nitrogen excess and ammonia is assimilated by the alanine dehydrogenase (AlaDH) pathway. We postulate that 'Chlorochromatium aggregatum' originated from a parasitic interaction where the N 2 fixation capacity of the chlorobia would be enhanced by injection of 2-oxoglutarate from the b-proteobacterium via the periplasm. This consortium would have the advantage of motility, which is fundamental to a phototrophic bacterium, and the syntrophy of nitrogen and carbon sources.

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“…Novelty-generating genetic combinations have produced a variety of evolutionary outcomes at different hierarchical levels (26). Examples include domain sharing between gene families (27), transfer of adaptive genes in prokaryotic genomes (28)(29)(30)(31)(32), pangenomes (33), and sharing of transposases (34), integron gene cassettes (29), plasmids (35), and phages (28,31) within genetic exchange communities (36); bacterial consortia, such as Chlorochromatium aggregatum, with partners undergoing synchronized separate cellular divisions (37); and endosymbiotic gene transfer (38,39).…”

mentioning

confidence: 99%

Evolutionary analyses of non-genealogical bonds produced by introgressive descent

Bapteste

Lopez

Bouchard

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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All evolutionary biologists are familiar with evolutionary units that evolve by vertical descent in a tree-like fashion in single lineages. However, many other kinds of processes contribute to evolutionary diversity. In vertical descent, the genetic material of a particular evolutionary unit is propagated by replication inside its own lineage. In what we call introgressive descent, the genetic material of a particular evolutionary unit propagates into different host structures and is replicated within these host structures. Thus, introgressive descent generates a variety of evolutionary units and leaves recognizable patterns in resemblance networks. We characterize six kinds of evolutionary units, of which five involve mosaic lineages generated by introgressive descent. To facilitate detection of these units in resemblance networks, we introduce terminology based on two notions, P3s (subgraphs of three nodes: A, B, and C) and mosaic P3s, and suggest an apparatus for systematic detection of introgressive descent. Mosaic P3s correspond to a distinct type of evolutionary bond that is orthogonal to the bonds of kinship and genealogy usually examined by evolutionary biologists. We argue that recognition of these evolutionary bonds stimulates radical rethinking of key questions in evolutionary biology (e.g., the relations among evolutionary players in very early phases of evolutionary history, the origin and emergence of novelties, and the production of new lineages). This line of research will expand the study of biological complexity beyond the usual genealogical bonds, revealing additional sources of biodiversity. It provides an important step to a more realistic pluralist treatment of evolutionary complexity.biodiversity structure | evolutionary transitions | lateral gene transfer | network of life | symbiosis

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The Phototrophic Consortium “Chlorochromatium aggregatum” – A Model for Bacterial Heterologous Multicellularity

Cited by 25 publications

References 26 publications

Protein networks identify novel symbiogenetic genes resulting from plastid endosymbiosis

Protein networks identify novel symbiogenetic genes resulting from plastid endosymbiosis

Metabolic analysis of Chlorobium chlorochromatii CaD3 reveals clues of the symbiosis in ‘Chlorochromatium aggregatum’

Evolutionary analyses of non-genealogical bonds produced by introgressive descent

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