scholarly journals Metabolic differences between symbiont subpopulations in the deep-sea tubeworm Riftia pachyptila

2020 ◽  
Author(s):  
Tjorven Hinzke ◽  
Manuel Kleiner ◽  
Mareike Meister ◽  
Rabea Schlüter ◽  
Christian Hentschker ◽  
...  
Keyword(s):  
Carbon Fixation ◽  
Statistical Evaluation ◽  
Gradient Centrifugation ◽  
Riftia Pachyptila ◽  
Metabolic Diversity ◽  
Host Animal ◽  
Host Interaction ◽  
Sulfur Oxidizing ◽  
Differentiation Stage ◽  
Vent Tube

AbstractThe hydrothermal vent tube worm Riftia pachyptila lives in intimate symbiosis with intracellular sulfur-oxidizing gammaproteobacteria. Although the symbiont population consists of a single 16S rRNA phylotype, bacteria in the same host animal exhibit a remarkable degree of metabolic diversity: They simultaneously utilize two carbon fixation pathways and various energy sources and electron acceptors. Whether these multiple metabolic routes are employed in the same symbiont cells, or rather in distinct symbiont subpopulations, was unclear. As Riftia symbionts vary considerably in cell size and shape, we enriched individual symbiont cell sizes by density gradient centrifugation in order to test whether symbiont cells of different sizes show different metabolic profiles. Metaproteomic analysis and statistical evaluation using clustering and random forests, supported by microscopy and flow cytometry, strongly suggest that Riftia symbiont cells of different sizes represent metabolically dissimilar stages of a physiological differentiation process: Small symbionts actively divide and may establish cellular symbiont-host interaction, as indicated by highest abundance of the cell division key protein FtsZ and highly abundant chaperones and porins in this initial phase. Large symbionts, on the other hand, apparently do not divide, but still replicate DNA, leading to DNA endoreduplication. Highest abundance of enzymes for CO2 fixation, carbon storage and biosynthesis in large symbionts indicates that in this late differentiation stage the symbiont’s metabolism is efficiently geared towards the production of organic material. We propose that this division of labor between smaller and larger symbionts benefits the productivity of the symbiosis as a whole.

scholarly journals Bacterial symbiont subpopulations have different roles in a deep-sea symbiosis

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Tjorven Hinzke ◽  
Manuel Kleiner ◽  
Mareike Meister ◽  
Rabea Schlüter ◽  
Christian Hentschker ◽  
...  
Keyword(s):  
Deep Sea ◽  
Hydrothermal Vent ◽  
Carbon Fixation ◽  
Density Gradient Centrifugation ◽  
Gradient Centrifugation ◽  
Bacterial Symbiont ◽  
Riftia Pachyptila ◽  
Physiological Diversity ◽  
Host Interaction ◽  
Sulfur Oxidizing

The hydrothermal vent tubeworm Riftia pachyptila hosts a single 16S rRNA phylotype of intracellular sulfur-oxidizing symbionts, which vary considerably in cell morphology and exhibit a remarkable degree of physiological diversity and redundancy, even in the same host. To elucidate whether multiple metabolic routes are employed in the same cells or rather in distinct symbiont subpopulations, we enriched symbionts according to cell size by density gradient centrifugation. Metaproteomic analysis, microscopy, and flow cytometry strongly suggest that Riftia symbiont cells of different sizes represent metabolically dissimilar stages of a physiological differentiation process: While small symbionts actively divide and may establish cellular symbiont-host interaction, large symbionts apparently do not divide, but still replicate DNA, leading to DNA endoreduplication. Moreover, in large symbionts, carbon fixation and biomass production seem to be metabolic priorities. We propose that this division of labor between smaller and larger symbionts benefits the productivity of the symbiosis as a whole.

scholarly journals Genetic evidence for two carbon fixation pathways in symbiotic and free-living bacteria: The Calvin-Benson-Bassham cycle and the reverse tricarboxylic acid cycle

2018 ◽  
Author(s):  
Maxim Rubin-Blum ◽  
Nicole Dubilier ◽  
Manuel Kleiner
Keyword(s):  
Carbon Fixation ◽  
Tricarboxylic Acid Cycle ◽  
Electron Flow ◽  
Tricarboxylic Acid ◽  
Riftia Pachyptila ◽  
Heterodisulfide Reductase ◽  
Free Living ◽  
Sulfur Oxidizer ◽  
Potential Benefits ◽  
Sulfur Oxidizing

AbstractVery few bacteria are able to fix carbon via both the reverse tricarboxylic acid (rTCA) and the Calvin-Benson-Bassham (CBB) cycles, such as symbiotic, sulfur-oxidizing bacteria that are the sole carbon source for the marine tubeworm Riftia pachyptila, the fastest growing invertebrate. To date, this co-existence of two carbon fixation pathways had not been found in a cultured bacterium and could thus not be studied in detail. Moreover, it was not clear if these two pathways were encoded in the same symbiont individual, or if two symbiont populations, each with one of the pathways, co-existed within tubeworms. With comparative genomics, we show that Thioflavicoccus mobilis, a cultured, free-living gammaproteobacterial sulfur oxidizer, possesses the genes for both carbon fixation pathways. Here, we also show that both the CBB and rTCA pathways are likely encoded in the genome of the sulfur-oxidizing symbiont of the tubeworm Escarpia laminata from deep-sea asphalt volcanoes in the Gulf of Mexico. Finally, we provide genomic and transcriptomic data suggesting a potential electron flow towards the rTCA cycle carboxylase 2-oxoglutarate:ferredoxin oxidoreductase, via a rare variant of NADH dehydrogenase/heterodisulfide reductase. This electron bifurcating complex, together with NAD(P)+ transhydrogenase and Na+ translocating Rnf membrane complexes may improve the efficiency of the rTCA cycle in both the symbiotic and the free-living sulfur oxidizer.ImportancePrimary production on Earth is dependent on autotrophic carbon fixation, which leads to the incorporation of carbon dioxide into biomass. Multiple metabolic pathways have been described for autotrophic carbon fixation, but most autotrophic organisms were assumed to have the genes for only one of these pathways. Our finding of a cultivable bacterium with two carbon fixation pathways in its genome opens the possibility to study the potential benefits of having two pathways and the interplay between these pathways. Additionally, this will allow the investigation of the unusual, and potentially very efficient mechanism of electron flow that could drive the rTCA cycle in these autotrophs. Such studies will deepen our understanding of carbon fixation pathways and could provide new avenues for optimizing carbon fixation in biotechnological applications.

scholarly journals Expanded Phylogenetic Diversity and Metabolic Flexibility of Mercury-Methylating Microorganisms

mSystems ◽  
2020 ◽  
Vol 5 (4) ◽  
Author(s):  
Elizabeth A. McDaniel ◽  
Benjamin D. Peterson ◽  
Sarah L. R. Stevens ◽  
Patricia Q. Tran ◽  
Karthik Anantharaman ◽  
...  
Keyword(s):  
Phylogenetic Diversity ◽  
Large Scale ◽  
Carbon Fixation ◽  
Anaerobic Bacteria ◽  
Inorganic Mercury ◽  
Metal Resistance ◽  
Metabolic Flexibility ◽  
Metabolic Diversity ◽  
Content Type ◽  
Methylmercury Production

ABSTRACT Methylmercury is a potent bioaccumulating neurotoxin that is produced by specific microorganisms that methylate inorganic mercury. Methylmercury production in diverse anaerobic bacteria and archaea was recently linked to the hgcAB genes. However, the full phylogenetic and metabolic diversity of mercury-methylating microorganisms has not been fully unraveled due to the limited number of cultured experimentally verified methylators and the limitations of primer-based molecular methods. Here, we describe the phylogenetic diversity and metabolic flexibility of putative mercury-methylating microorganisms by hgcAB identification in publicly available isolate genomes and metagenome-assembled genomes (MAGs) as well as novel freshwater MAGs. We demonstrate that putative mercury methylators are much more phylogenetically diverse than previously known and that hgcAB distribution among genomes is most likely due to several independent horizontal gene transfer events. The microorganisms we identified possess diverse metabolic capabilities spanning carbon fixation, sulfate reduction, nitrogen fixation, and metal resistance pathways. We identified 111 putative mercury methylators in a set of previously published permafrost metatranscriptomes and demonstrated that different methylating taxa may contribute to hgcA expression at different depths. Overall, we provide a framework for illuminating the microbial basis of mercury methylation using genome-resolved metagenomics and metatranscriptomics to identify putative methylators based upon hgcAB presence and describe their putative functions in the environment. IMPORTANCE Accurately assessing the production of bioaccumulative neurotoxic methylmercury by characterizing the phylogenetic diversity, metabolic functions, and activity of methylators in the environment is crucial for understanding constraints on the mercury cycle. Much of our understanding of methylmercury production is based on cultured anaerobic microorganisms within the Deltaproteobacteria, Firmicutes, and Euryarchaeota. Advances in next-generation sequencing technologies have enabled large-scale cultivation-independent surveys of diverse and poorly characterized microorganisms from numerous ecosystems. We used genome-resolved metagenomics and metatranscriptomics to highlight the vast phylogenetic and metabolic diversity of putative mercury methylators and their depth-discrete activities in thawing permafrost. This work underscores the importance of using genome-resolved metagenomics to survey specific putative methylating populations of a given mercury-impacted ecosystem.

ATP sulfurylase from trophosome tissue of Riftia pachyptila (hydrothermal vent tube worm)

1991 ◽  
Vol 290 (1) ◽  
pp. 66-78 ◽  
Author(s):  
Franco Renosto ◽  
Robert L. Martin ◽  
Jeffrey L. Borrell ◽  
Douglas C. Nelson ◽  
Irwin H. Segel
Keyword(s):  
Hydrothermal Vent ◽  
Riftia Pachyptila ◽  
Atp Sulfurylase ◽  
Vent Tube

Production and respiration in the Red Sea coral Stylophora pistillata as a function of depth

1984 ◽  
Vol 222 (1227) ◽  
pp. 215-230 ◽  
Keyword(s):  
Carbon Fixation ◽  
Algal Cell ◽  
Unit Surface Area ◽  
Fixed Carbon ◽  
Host Animal ◽  
Direct Function ◽  
Stylophora Pistillata ◽  
Carbon Availability ◽  
Branch Density ◽  
Average Size

Colony morphology, rates of production and respiration, translocation of carbon from symbiotic algae to host, and the daily contribution of carbon fixed by zooxanthellae to animal respiration demands (CZAR) in phenotypes of Stylophora pistillata from 3 and 35 m were compared. Corals from 35 m showed an increase in branch density, a decrease in zooxanthellae density, and an increase in chlorophyll a per algal cell when compared to colonies from 3m. These changes are explained as adaptations to limited photosynthetically active radiation at the deeper depth. Photosynthetic efficiency was higher at 35 m, as evidenced by a production rate 25% that at 3 m, but with light only about 8% that of shallow water irradiance. Respiration of deeper corals decreased by a half. A depth-specific respiratory decline was displayed by both the algae and the animal fractions. Decreased coral animal respiration appears to be a direct function of decreased photosynthetically fixed carbon availability, and to be an immediate response to daily carbon input. Decreased carbon availability to the host animal at 35 m was a consequence of both decreased net carbon fixation and decreased percentage of net fixed carbon translocated to the host. The daily CZAR at 35 m was less than half that at 3m. Mean CZAR at 35 m was 78%, suggesting that deeper corals have an obligate requirement for heterotrophically obtained carbon. By contrast, corals from 3m, which displayed a mean CZAR of 157%, appeared to be photo trophic with respect to carbon required for respiration. Altered trophic strategies with depth were confirmed by daily carbon budgets calculated for average size corals from both depths. Multiple correlation tests of all parameters confirmed the utility of expressing production and respiration measures in terms of unit surface area. However, significant correlations with other normalizing parameters were found, and their usefulness discussed.

Sulfide acquisition by the vent worm Riftia pachyptila appears to be via uptake of HS-, rather than H2S.

1997 ◽  
Vol 200 (20) ◽  
pp. 2609-2616
Author(s):  
S K Goffredi ◽  
J J Childress ◽  
N T Desaulniers ◽  
F J Lallier
Keyword(s):  
Hydrothermal Vents ◽  
Carbon Fixation ◽  
Extracellular Fluid ◽  
High Growth ◽  
Riftia Pachyptila ◽  
Sulfide Toxicity ◽  
Sulfide Inhibition ◽  
Chemosynthetic Bacteria ◽  
Preferential Uptake ◽  
Very High

Deep-sea hydrothermal vents are home to a variety of invertebrate species, many of which host chemosynthetic bacteria in unusual symbiotic arrangements. The vent tubeworm Riftia pachyptila (Vestimentifera) relies upon internal chemolithoautotrophic bacterial symbionts to support its large size and high growth rates. Because of this, R. pachyptila must supply sulfide to the bacteria, which are far removed from the external medium. Internal H2S ([H2S+HS-+S2-]) can reach very high levels in R. pachyptila (2-12mmoll-1 in the vascular blood), most of which is bound to extracellular hemoglobins. The animal can potentially take up sulfide from the environment via H2S diffusion or via mediated uptake of HS-, or both. It was expected that H2S diffusion would be the primary sulfide acquisition mechanism, paralleling the previously demonstrated preferential uptake of CO2. Our data show, however, that the uptake of HS- is the primary mechanism used by R. pachyptila to obtain sulfide and that H2S diffusion into the worm apparently proceeds at a much slower rate than expected. This unusual mechanism may have evolved because HS- is less toxic than H2S and because HS- uptake decouples sulfide and inorganic carbon acquisition. The latter occurs via the diffusion of CO2 at very high rates due to the maintenance of an alkaline extracellular fluid pH. H2S accumulation is limited, however, to sulfide that can be bound by the hemoglobins, protecting the animal from sulfide toxicity and the symbionts from sulfide inhibition of carbon fixation.

Hemoglobin Kinetics of the Galapagos Rift Vent Tube Worm Riftia pachyptila Jones (Pogonophora; Vestimentifera)

Science ◽  
1981 ◽  
Vol 213 (4505) ◽  
pp. 344-346 ◽  
Author(s):  
J. B. WITTENBERG ◽  
R. J. MORRIS ◽  
Q. H. GIBSON ◽  
M. L. JONES
Keyword(s):  
Riftia Pachyptila ◽  
Vent Tube ◽  
Galapagos Rift ◽  
Kinetics Of
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