New Genomic Insights into “Entotheonella” Symbionts in Theonella swinhoei: Mixotrophy, Anaerobic Adaptation, Resilience, and Interaction

Liu, Fang; Li, Jinlong; Gao, Feng; Li, Zhiyong

doi:10.3389/fmicb.2016.01333

Cited by 24 publications

(24 citation statements)

References 68 publications

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“…Entotheonella strains described here (99.9% average nucleotide identity), and should thus belong to the same candidate species. In contrast to our analysis, Liu et al (52) claim that they identified the CalvinBenson cycle for CO 2 fixation (via ribulose-1,5-bisphosphate carboxylase), candidates for crassulacean acid metabolism (a phenomenon exclusively known in plants), a type VI secretion system, and a complete system for endospore formation. Despite extensive manual and automated reinvestigation of our dataset as well as the sequence data provided for the Chinese sponge, we cannot find any evidence for these genomic features.…”

Section: Resultscontrasting

confidence: 99%

Insights into the lifestyle of uncultured bacterial natural product factories associated with marine sponges

Lackner

Peters

Helfrich

et al. 2017

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

126

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The as-yet uncultured filamentous bacteria "Candidatus Entotheonella factor" and "Candidatus Entotheonella gemina" live associated with the marine sponge Theonella swinhoei Y, the source of numerous unusual bioactive natural products. Belonging to the proposed candidate phylum "Tectomicrobia," Candidatus Entotheonella members are only distantly related to any cultivated organism. The Ca. E. factor has been identified as the source of almost all polyketide and modified peptides families reported from the sponge host, and both Ca. Entotheonella phylotypes contain numerous additional genes for as-yet unknown metabolites. Here, we provide insights into the biology of these remarkable bacteria using genomic, (meta)proteomic, and chemical methods. The data suggest a metabolic model of Ca. Entotheonella as facultative anaerobic, organotrophic organisms with the ability to use methanol as an energy source. The symbionts appear to be auxotrophic for some vitamins, but have the potential to produce most amino acids as well as rare cofactors like coenzyme F 420 . The latter likely accounts for the strong autofluorescence of Ca. Entotheonella filaments. A large expansion of protein families involved in regulation and conversion of organic molecules indicates roles in host-bacterial interaction. In addition, a massive overrepresentation of members of the luciferase-like monooxygenase superfamily points toward an important role of these proteins in Ca. Entotheonella. Furthermore, we performed mass spectrometric imaging combined with fluorescence in situ hybridization to localize Ca. Entotheonella and some of the bioactive natural products in the sponge tissue. These metabolic insights into a new candidate phylum offer hints on the targeted cultivation of the chemically most prolific microorganisms known from microbial dark matter.

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Section: Resultscontrasting

confidence: 99%

Insights into the lifestyle of uncultured bacterial natural product factories associated with marine sponges

Lackner

Peters

Helfrich

et al. 2017

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

126

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“…Urease genes were also found in other spongeassociated microbial genomes and microbiomes (Hallam et al, 2006;Siegl et al, 2011;Bayer et al, 2014;Liu et al, 2016). Together with the phylogenetic diversity found for ureC genes and transcripts found in the sponge Xestospongia testudinaria (Su et al, 2013), these data indicate that urea degradation is a common trait of sponge-associated microorganisms.…”

Section: Metabolic Features Of Diatoms and The Spongementioning

confidence: 53%

Integrated metabolism in sponge–microbe symbiosis revealed by genome-centered metatranscriptomics

et al. 2017

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Despite an increased understanding of functions in sponge microbiomes, the interactions among the symbionts and between symbionts and host are not well characterized. Here we reconstructed the metabolic interactions within the sponge Cymbastela concentrica microbiome in the context of functional features of symbiotic diatoms and the host. Three genome bins (CcPhy, CcNi and CcThau) were recovered from metagenomic data of C. concentrica, belonging to the proteobacterial family Phyllobacteriaceae, the Nitrospira genus and the thaumarchaeal order Nitrosopumilales. Gene expression was estimated by mapping C. concentrica metatranscriptomic reads. Our analyses indicated that CcPhy is heterotrophic, while CcNi and CcThau are chemolithoautotrophs. CcPhy expressed many transporters for the acquisition of dissolved organic compounds, likely available through the sponge's filtration activity and symbiotic carbon fixation. Coupled nitrification by CcThau and CcNi was reconstructed, supported by the observed close proximity of the cells in fluorescence in situ hybridization. CcPhy facultative anaerobic respiration and assimilation by diatoms may consume the resulting nitrate. Transcriptional analysis of diatom and sponge functions indicated that these organisms are likely sources of organic compounds, for example, creatine/creatinine and dissolved organic carbon, for other members of the symbiosis. Our results suggest that organic nitrogen compounds, for example, creatine, creatinine, urea and cyanate, fuel the nitrogen cycle within the sponge. This study provides an unprecedented view of the metabolic interactions within sponge-microbe symbiosis, bridging the gap between cell-and community-level knowledge.

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“…CC BY 4.0 License. Fiore et al, 2015;Han et al, 2013;Li et al, 2014;Liu et al, 2016;Liu et al, 2012;Webster and Taylor, 2012;Zhang et al, 2013;Zhuang et al, 2018).…”

Section: Denitrification As a Common Feature Of Cold-water Spongesmentioning

confidence: 99%

Deep-sea sponge grounds as nutrient sinks: High denitrification rates in boreo-arctic sponges

Rooks

Fang

Mørkved

et al. 2019

Preprint

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Abstract. Sponges are commonly known as general nutrient providers for the marine ecosystem, recycling organic matter into various forms of bio-available nutrients such as ammonium and nitrate. In this study we challenge this view. We show that nutrient removal through microbial denitrification is a common feature in six cold-water sponge species from boreal and Arctic sponge grounds. Denitrification rates were quantified by incubating sponge tissue sections with 15NO3- &#8211; amended oxygen saturated seawater, mimicking conditions in pumping sponges, and de-oxygenated seawater, mimicking non-pumping sponges. Rates of anaerobic ammonium oxidation (anammox) using incubations with 15NH4+ could not be detected. Denitrification rates of the different sponge species ranged from 0 to 114&#8201;nmol&#8201;N&#8201;cm-3&#8201;sponge&#8201;day-1 under oxic conditions, and from 47 to 342&#8201;nmol&#8201;N&#8201;cm-3&#8201;sponge&#8201;day-1 under anoxic conditions. An exponential relationship between the highest potential rates of denitrification (in the absence of oxygen) and the species-specific abundances of nirS and nirK genes encoding nitrite reductase, a key enzyme for denitrification, suggests that the denitrifying community in these sponge species is both prepared and optimized for denitrification. The lack of a lag phase in the linear accumulation of the 15N labelled N2 gas in any of our tissue incubations is another indicator for an active community of denitrifiers in the investigated sponge species. High rates for coupled nitrification-denitrification (up to 89&#8201;% of nitrate reduction in the presence of oxygen) shows that under these conditions, the NO3- reduced in denitrification was primarily derived from nitrification within the sponge, directly coupling organic matter degradation and nitrification to denitrification in sponge tissues. Under anoxic condition when nitrification was not possible, nitrate to fuel the much higher denitrification rates had to be retrieved directly from the seawater. The lack of nifH genes encoding nitrogenase, the key enzyme for nitrogen fixation, shows that the nitrogen cycle is not closed in the sponge grounds. The denitrified nitrogen, no matter of its origin, is then no longer available as a nutrient for the marine ecosystem. Considering average sponge biomasses on typical boreal and Arctic sponge grounds, our sponge denitrification rates reveal areal denitrification rates of 0.8&#8201;mmol&#8201;N&#8201;m-2&#8201;day-1 assuming non-pumping sponges and still 0.3&#8201;mmol&#8201;N&#8201;m-2&#8201;day-1 assuming pumping sponges. This is well within the range of denitrification rates of continental shelf sediments. For the most densely populated boreal sponge grounds we calculated denitrification rates of up to 2&#8201;mmol&#8201;N&#8201;m-2&#8201;day-1, which is comparable to rates in coastal sediments. Increased future impact of sponge grounds by anthropogenic stressors reducing sponge pumping activity and further stimulating sponge anaerobic processes may thus lead to that deep-sea sponge grounds change their role in the marine ecosystem from nutrient sources to nutrient sinks.

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New Genomic Insights into “Entotheonella” Symbionts in Theonella swinhoei: Mixotrophy, Anaerobic Adaptation, Resilience, and Interaction

Cited by 24 publications

References 68 publications

Insights into the lifestyle of uncultured bacterial natural product factories associated with marine sponges

Insights into the lifestyle of uncultured bacterial natural product factories associated with marine sponges

Integrated metabolism in sponge–microbe symbiosis revealed by genome-centered metatranscriptomics

Deep-sea sponge grounds as nutrient sinks: High denitrification rates in boreo-arctic sponges

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