Intracellular Spheroid Bodies of Rhopalodia gibba Have Nitrogen-Fixing Apparatus of Cyanobacterial Origin

Prechtl, Julia; Christoph, Kneip; Lockhart, Peter J.; Wenderoth, Klaus; Maier, Uwe‐G.

doi:10.1093/molbev/msh086

Cited by 125 publications

(113 citation statements)

References 19 publications

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“…With exception of marine Protokeelia species, rhopalodiacean diatoms can be seen widely in freshwater habitats. The cyanobacterial symbionts, so-called "spheroid bodies", has been found in species of Rhopalodia and Epithemia, and previous observations of the R. gibba spheroid body (4-6 mm in width, 5-7 mm in length) showed that the symbiont resides in the host cytoplasm and has two envelope membranes with putatively distinct origins -the outer one was derived from the eukaryotic host cell, while the inner one is the plasmamembrane of the symbiont [8][9][10]. It has been shown that the number of the spheroid bodies per diatom cell can vary depending on the availability of nitrogen compounds in culture media [11].…”

Section: Spheroid Bodies In Rhopalodiacean Diatomsmentioning

confidence: 99%

Unique genome evolution in an intracellular N2-fixing symbiont of a rhopalodiacean diatom

Nakayama

Inagaki

2014

Acta Soc Bot Pol

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Cyanobacteria, the major photosynthetic prokaryotic lineage, are also known as a major nitrogen fixer in nature. N 2 -fixing cyanobacteria are frequently found in symbioses with various types of eukaryotes and supply fixed nitrogen compounds to their eukaryotic hosts, which congenitally lack N 2 -fixing abilities. Diatom species belonging to the family Rhopalodiaceae also possess cyanobacterial symbionts called spheroid bodies. Unlike other cyanobacterial N 2 -fixing symbionts, the spheroid bodies reside in the cytoplasm of the diatoms and are inseparable from their hosts. Recently, the first spheroid body genome from a rhopalodiacean diatom has been completely sequenced. Overall features of the genome sequence showed significant reductive genome evolution resulting in a diminution of metabolic capacity. Notably, despite its cyanobacterial origin, the spheroid body was shown to be truly incapable of photosynthesis implying that the symbiont energetically depends on the host diatom. The comparative genome analysis between the spheroid body and another N 2 -fixing symbiotic cyanobacterial group corresponding to the UCYN-A phylotypes -both were derived from cyanobacteria closely related to genus Cyanothece -revealed that the two symbionts are on similar, but explicitly distinct tracks of reductive evolution. Intimate symbiotic relationships linked by nitrogen fixation as seen in rhopalodiacean diatoms may help us better understand the evolution and mechanisms of bacterium-eukaryote endosymbioses.

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Section: Spheroid Bodies In Rhopalodiacean Diatomsmentioning

confidence: 99%

Unique genome evolution in an intracellular N2-fixing symbiont of a rhopalodiacean diatom

Nakayama

Inagaki

2014

Acta Soc Bot Pol

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“…Also, while the association between shipworms or diatoms and their diazotrophs is obligatory and can be described as a symbiosis (Prechtl, 2004), no study has actually shown if corals and diazotrophs form a facultative association or a real symbiosis. On one hand, Lema et al (2012Lema et al ( , 2014a observed high species specificity in the diazotrophic bacteria that dominated the tissue of all coral species investigated, as well as a spatial and temporal consistency in the diazotroph community of the Acropora millepora microbiome.…”

Section: Diazotroph-host Symbioses/associations In Coral Reef Ecosystemsmentioning

confidence: 99%

Diazotrophs: Overlooked Key Players within the Coral Symbiosis and Tropical Reef Ecosystems?

2017

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Coral reefs are highly productive ecosystems thriving in nutrient-poor waters. Their productivity depends largely on the availability of nitrogen, the proximate limiting nutrient for primary production. In reefs, the major nitrogen pathways include regeneration, nitrification, ammonification and dinitrogen (N 2 ) fixation. N 2 fixation is performed by prokaryotes called "diazotrophs" that abound in coral rubbles, sandy bottoms, microbial mats, or seagrass meadows. Corals, which are the main reef builders, have developed a partnership with dinoflagellates which transform dissolved inorganic nitrogen into amino acids and protein, and with diazotrophs to gain diazotrophically-derived nitrogen (DDN). Pioneering studies found active diazotrophic cyanobacteria in the corals' mucus and/or tissue, and later high throughput sequencing efforts have described diverse communities of non-cyanobacterial diazotrophs associated with scleractinian corals. Yet, the metabolic processes behind these associations and how they benefit corals are currently not well understood. While genomic studies describe the diversity of diazotrophs and isotopic tracer experiments quantify N 2 fixation rates, combined advanced methods are needed to elucidate the mechanisms behind the transfer of DDN to the coral holobiont and whether these mechanisms change according to the identity of the diazotrophs or coral species. Here we review our current knowledge on N 2 fixation in corals: the diversity and localization of diazotrophs in the coral holobiont, the environmental factors controlling N 2 fixation, the fate of DDN within the coral symbiosis as well as its potential role in coral resilience. We finally summarize the unknowns: are the diversity, abundance and localization of diazotrophs within the holobiont species-and/or site-specific? Do they have an impact on DDN production? What are the metabolic mechanisms implicated? Do they change spatially, temporally or according to environmental factors? We encourage scientists to undertake research efforts to tackle these questions in order to shed light on nitrogen cycling in reef ecosystems and to understand if coral-associated N 2 fixation can improve coral's resilience in the face of climate change.

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“…There are other examples of highly reduced cyanobacterial endosymbionts, such as Candidatus Atelocyanobacterium thalassa living symbiotically with a haptophyte alga [85] or the "spheroid bodies" in rhopalodiacean diatoms [86,87]. However, these symbionts lost their ability to perform oxygenic photosynthesis and their main function is thought to be nitrogen fixation.…”

Section: Import Of Nuclear-encoded Proteins Into the Chromatophorementioning

confidence: 99%

Paulinella chromatophora – rethinking the transition from endosymbiont to organelle

Nowack

2014

Acta Soc Bot Pol

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The evolution of plastidsPrimary plastids, the photosynthetic organelles of Plantae (i.e. green algae/land plants, red algae, and glaucophytes) evolved more than 1 billion years ago (gya) through the endosymbiotic uptake of a cyanobacterium by a heterotrophic protist host [1][2][3]. Photosynthetic carbon fixation from the newly acquired plastid relieved the host from its dependency on the continuous uptake of organic carbon molecules from the environment. In addition to photosynthetic carbon fixation, plastids provide other beneficial metabolic functions to the plant/algal cell such as the assimilation of ammonia and sulfate into amino acids [4], assembly of iron-sulfur clusters [5], de novo biosynthesis of fatty acids [6], isopentenyl diphosphate (IPP) [7], and aromatic amino acids [8]; and they contribute to pathways that are distributed over several compartments, such as photorespiration and biosynthesis of pyrimidines and folates [9][10][11].Evolution of plastids was accompanied by a strong reduction of the size of the cyanobacterial genome and the transfer of thousands of cyanobacterial genes into the host nuclear genome, a process termed endosymbiotic gene transfer (EGT) [12,13]. This resulted in proteins localized to the cyanobacterium, now a full-fledged plastid, being synthesized in the cytoplasm and then imported into the plastid through a sophisticated import machinery (the TIC/ TOC complex; short for: translocon of the inner and outer chloroplast membranes) targeted by N-terminal transit peptides [14]. A multitude of solute transporters underlie the intricate metabolic crosstalk between plastid and the surrounding cell by controlling fluxes of metabolites and ions through the double membrane system that delimits the plastid [15][16][17]. Signaling pathways from and to the plastid communicate environmental cues and the metabolic and developmental status of different compartments within the plant/algal cell [18,19]. An interplay of eukaryote-and cyanobacterium-derived proteins coordinate plastid division with the host cell cycle [20].Following the establishment of primary plastids in Plantae, photosynthetic ability spread to other eukaryotic lineages through secondary endosymbioses [21,22]. In secondary endosymbioses a red or green alga served as an endosymbiont, leading to the establishment of secondary plastids in heterokontophytes (stramenopiles), cryptophytes, haptophytes, dinoflagellates, apicomplexa, chlorarachniophytes, and euglenophytes. In most cases the only remnant of the eukaryotic symbiont is one or two extra membranes that surround the secondary plastid. The nuclear genome of the * Email: e.nowack@uni-duesseldorf.deHandling Editor: Andrzej Bodył INVITED REVIEW Acta Soc Bot Pol 83(4): 387-397 DOI: 10.5586/asbp.2014.049 Received: 2014-11-16 Accepted: 2014-12-19 Published electronically: 2014 Paulinella chromatophora -rethinking the transition from endosymbiont to organelle Eva C.M. Nowack* Department of Biology, Heinrich-Heine-Universität Düsseldorf, Universitätsstrasse 1, 40225 Düsseldorf...

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Intracellular Spheroid Bodies of Rhopalodia gibba Have Nitrogen-Fixing Apparatus of Cyanobacterial Origin

Cited by 125 publications

References 19 publications

Unique genome evolution in an intracellular N2-fixing symbiont of a rhopalodiacean diatom

Unique genome evolution in an intracellular N2-fixing symbiont of a rhopalodiacean diatom

Diazotrophs: Overlooked Key Players within the Coral Symbiosis and Tropical Reef Ecosystems?

Paulinella chromatophora – rethinking the transition from endosymbiont to organelle

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