Genome of ‘<i>Ca.</i> Desulfovibrio trichonymphae’, an H2-oxidizing bacterium in a tripartite symbiotic system within a protist cell in the termite gut

Kuwahara, Hiroya; Yuki, Masahiro; Izawa, Kazuki; Ohkuma, Moriya; Hongoh, Yuichi

doi:10.1038/ismej.2016.143

Cited by 37 publications

(43 citation statements)

References 55 publications

(74 reference statements)

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“…H 2 cycling is a process thought to occur within an individual cell (Odom & Peck, ), but it is also possible that this occurs as a syntrophic transfer of H 2 from the Dbulb to Dbact symbionts. Removal of H 2 produced by a bacterial cosymbiont was also proposed for the deltaproteobacterial episymbiont of a parabasalid protist inhabiting termite guts (Kuwahara, Yuki, Izawa, Ohkuma, & Hongoh, ). Thus, consortia between protists and multiple prokaryotic partners may not exclusively represent metabolic relationships solely between the host and individual symbiont types.…”

Section: Resultsmentioning

confidence: 96%

Insights into the metabolic functioning of a multipartner ciliate symbiosis from oxygen‐depleted sediments

et al. 2018

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Symbioses between anaerobic or microaerophilic protists and prokaryotes are common in anoxic and oxygen-depleted habitats ranging from marine sediments to gastrointestinal tracts. Nevertheless, little is known about the mechanisms of metabolic interaction between partners. In these putatively syntrophic associations, consumption of fermentative end products (e.g., hydrogen) by the prokaryotic symbionts is thought to facilitate protistan anaerobic metabolism. Here, we employed metagenomic and metatranscriptomic sequencing of a microaerophilic or anaerobic karyorelictid ciliate and its prokaryotic symbionts from oxygen-depleted Santa Barbara Basin (CA, USA) sediments to assess metabolic coupling within this consortium. This sequencing confirmed the predominance of deltaproteobacterial symbionts from the Families Desulfobacteraceae and Desulfobulbaceae and suggested active symbiont reduction of host-provided sulphate, transfer of small organic molecules from host to symbionts and hydrogen cycling among the symbionts. In addition, patterns of gene expression indicated active cell division by the symbionts, their growth via autotrophic processes and nitrogen exchange with the ciliate host. Altogether, this research underscores the importance of symbiont metabolism to host fermentative metabolism and, thus, likely its success in anoxic and low-oxygen habitats, but also suggests ciliate-associated prokaryotes play a role in important biogeochemical processes.

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Section: Resultsmentioning

confidence: 96%

Insights into the metabolic functioning of a multipartner ciliate symbiosis from oxygen‐depleted sediments

et al. 2018

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“…In our single-cell genome analysis of “ Ca. Gastranaerophilus termiticola” phylotype Tpq-Mel-01, no evidence was found to support the bacterium being directly involved in the hydrolysis of cellulose or hemicellulose, nitrogen fixation, the recycling of uric acids, reductive acetogenesis, or hydrogen oxidation, which are considered to be critical roles of gut bacteria for mutualism with the termite host ( 6 , 13 , 19 , 30 ). Thus, melainabacteria in the termite gut appear to be commensal, but still comprise a part of the microbiota specific to the guts of termites and cockroaches.…”

Section: Discussionmentioning

confidence: 99%

Phylogenetic Diversity and Single-Cell Genome Analysis of “<i>Melainabacteria</i>”, a Non-Photosynthetic Cyanobacterial Group, in the Termite Gut

Utami

Kuwahara

Murakami

et al. 2018

Microbes and environments

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Termite guts harbor diverse yet-uncultured bacteria, including a non-photosynthetic cyanobacterial group, the class “Melainabacteria”. We herein reported the phylogenetic diversity of “Melainabacteria” in the guts of diverse termites and conducted a single-cell genome analysis of a melainabacterium obtained from the gut of the termite Termes propinquus. We performed amplicon sequencing of 16S rRNA genes from the guts of 60 termite and eight cockroach species, and detected melainabacterial sequences in 48 out of the 68 insect species, albeit with low abundances (0.02–1.90%). Most of the melainabacterial sequences obtained were assigned to the order “Gastranaerophilales” and appeared to form clusters unique to termites and cockroaches. A single-cell genome of a melainabacterium, designated phylotype Tpq-Mel-01, was obtained using a fluorescence-activated cell sorter and whole genome amplification. The genome shared basic features with other melainabacterial genomes previously reconstructed from the metagenomes of human and koala feces. The bacterium had a small genome (~1.6 Mb) and possessed fermentative pathways possibly using sugars and chitobiose as carbon and energy sources, while the pathways for photosynthesis and carbon fixation were not found. The genome contained genes for flagellar components and chemotaxis; therefore, the bacterium is likely motile. A fluorescence in situ hybridization analysis showed that the cells of Tpq-Mel-01 and/or its close relatives are short rods with the dimensions of 1.1±0.2 μm by 0.5±0.1 μm; for these bacteria, we propose the novel species, “Candidatus Gastranaerophilus termiticola”. Our results provide fundamental information on “Melainabacteria” in the termite gut and expand our knowledge on this underrepresented, non-photosynthetic cyanobacterial group.

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“…Such types of interactions are not unprecedented and were recently proposed in protozoa in the gut of wood feeding termites. In the termite gut, the genome of one protozoa associated symbiont was shown to harbor the Wood–Ljungdahl pathway while another symbiont encodes for genes related to sulfate/fumarate reduction, another hydrogenotrophic activity found in the rumen ( Ikeda-Ohtsubo et al, 2016 ; Kuwahara et al, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

Exploring the Prokaryotic Community Associated With the Rumen Ciliate Protozoa Population

Levy

Jami

2018

Front. Microbiol.

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Ciliate protozoa are an integral part of the rumen microbiome and were found to exert a large effect on the rumen ecosystem itself as well as their host animal physiology. Part of these effects have been attributed to their ability to harbor a diverse ecto- and endo-symbiotic community of prokaryotic cells. Studies on the relationship between the protozoa population and their associated prokaryotic community in the rumen mainly focused on the methanogens, revealing that protozoa play a major role in enhancing methanogenesis potential. In contrast, little is known about the composition and function of the bacteria associated with rumen protozoa and the extent of this association. In this study, we characterize the prokaryotic communities associated with different protozoa populations and compare their structure to the free-living prokaryotic population residing in the cow rumen. We show that the overall protozoa associated prokaryotic community structure differs significantly compared to the free-living community in terms of richness and composition. The methanogens proportion was significantly higher in all protozoa populations compared to the free-living fraction, while the Lachnospiraceae was the most prevalent bacterial family in the protozoa associated bacterial communities. Several taxa not detected or detected in extremely low abundance in the free-living community were enriched in the protozoa associated bacterial community. These include members of the Endomicrobia class, previously identified as protozoa symbionts in the termite gut. Our results show that rumen protozoa harbor prokaryotic communities that are compositionally different from their surroundings, which may be the result of specific tropism between the prokaryotic community and protozoa.

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Genome of ‘Ca. Desulfovibrio trichonymphae’, an H2-oxidizing bacterium in a tripartite symbiotic system within a protist cell in the termite gut

Cited by 37 publications

References 55 publications

Insights into the metabolic functioning of a multipartner ciliate symbiosis from oxygen‐depleted sediments

Insights into the metabolic functioning of a multipartner ciliate symbiosis from oxygen‐depleted sediments

Phylogenetic Diversity and Single-Cell Genome Analysis of “<i>Melainabacteria</i>”, a Non-Photosynthetic Cyanobacterial Group, in the Termite Gut

Exploring the Prokaryotic Community Associated With the Rumen Ciliate Protozoa Population

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