scholarly journals Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO2Fixation

mBio ◽  
2019 ◽  
Vol 10 (3) ◽  
Author(s):  
Brandon K. B. Seah ◽  
Chakkiath Paul Antony ◽  
Bruno Huettel ◽  
Jan Zarzycki ◽  
Lennart Schada von Borzyskowski ◽  
...  
Keyword(s):  
Stable Isotope ◽  
Food Source ◽  
Carbon Fixation ◽  
Tricarboxylic Acid Cycle ◽  
Carbon Sources ◽  
Coastal Sediments ◽  
Carbon Stable Isotope ◽  
Main Food ◽  
Sulfur Oxidizing ◽  
Main Food Source

ABSTRACTSince the discovery of symbioses between sulfur-oxidizing (thiotrophic) bacteria and invertebrates at hydrothermal vents over 40 years ago, it has been assumed that autotrophic fixation of CO2by the symbionts drives these nutritional associations. In this study, we investigated “CandidatusKentron,” the clade of symbionts hosted byKentrophoros, a diverse genus of ciliates which are found in marine coastal sediments around the world. Despite being the main food source for their hosts, Kentron bacteria lack the key canonical genes for any of the known pathways for autotrophic carbon fixation and have a carbon stable isotope fingerprint that is unlike other thiotrophic symbionts from similar habitats. Our genomic and transcriptomic analyses instead found metabolic features consistent with growth on organic carbon, especially organic and amino acids, for which they have abundant uptake transporters. All known thiotrophic symbionts have converged on using reduced sulfur to gain energy lithotrophically, but they are diverse in their carbon sources. Some clades are obligate autotrophs, while many are mixotrophs that can supplement autotrophic carbon fixation with heterotrophic capabilities similar to those in Kentron. Here we show that Kentron bacteria are the only thiotrophic symbionts that appear to be entirely heterotrophic, unlike all other thiotrophic symbionts studied to date, which possess either the Calvin-Benson-Bassham or the reverse tricarboxylic acid cycle for autotrophy.IMPORTANCEMany animals and protists depend on symbiotic sulfur-oxidizing bacteria as their main food source. These bacteria use energy from oxidizing inorganic sulfur compounds to make biomass autotrophically from CO2, serving as primary producers for their hosts. Here we describe a clade of nonautotrophic sulfur-oxidizing symbionts, “CandidatusKentron,” associated with marine ciliates. They lack genes for known autotrophic pathways and have a carbon stable isotope fingerprint heavier than other symbionts from similar habitats. Instead, they have the potential to oxidize sulfur to fuel the uptake of organic compounds for heterotrophic growth, a metabolic mode called chemolithoheterotrophy that is not found in other symbioses. Although several symbionts have heterotrophic features to supplement primary production, in Kentron they appear to supplant it entirely.

scholarly journals Sulfur-oxidizing symbionts without canonical genes for autotrophic CO2fixation

2019 ◽  
Author(s):  
Brandon K. B. Seah ◽  
Chakkiath Paul Antony ◽  
Bruno Huettel ◽  
Jan Zarzycki ◽  
Lennart Schada von Borzyskowski ◽  
...  
Keyword(s):  
Stable Isotope ◽  
Hydrothermal Vents ◽  
Food Source ◽  
Carbon Fixation ◽  
Carbon Sources ◽  
Coastal Sediments ◽  
Carbon Stable Isotope ◽  
Main Food ◽  
Sulfur Oxidizing ◽  
Main Food Source

AbstractSince the discovery of symbioses between sulfur-oxidizing (thiotrophic) bacteria and invertebrates at hydrothermal vents over 40 years ago, it has been assumed that autotrophic fixation of CO2by the symbionts drives these nutritional associations. In this study, we investigatedCandidatusKentron, the clade of symbionts hosted byKentrophoros, a diverse genus of ciliates which are found in marine coastal sediments around the world. Despite being the main food source for their hosts, Kentron lack the key canonical genes for any of the known pathways for autotrophic fixation, and have a carbon stable isotope fingerprint unlike other thiotrophic symbionts from similar habitats. Our genomic and transcriptomic analyses instead found metabolic features consistent with growth on organic carbon, especially organic and amino acids, for which they have abundant uptake transporters. All known thiotrophic symbionts have converged on using reduced sulfur to generate energy lithotrophically, but they are diverse in their carbon sources. Some clades are obligate autotrophs, while many are mixotrophs that can supplement autotrophic carbon fixation with heterotrophic capabilities similar to those in Kentron. We have shown that Kentron are the only thiotrophic symbionts that appear to be entirely heterotrophic, unlike all other thiotrophic symbionts studied to date, which possess either the Calvin-Benson-Bassham or reverse tricarboxylic acid cycles for autotrophy.Significance StatementMany animals and protists depend on symbiotic sulfur-oxidizing bacteria as their main food source. These bacteria use energy from oxidizing inorganic sulfur compounds to make biomass autotrophically from CO2, serving as primary producers for their hosts. Here we describe apparently non-autotrophic sulfur symbionts called Kentron, associated with marine ciliates. They lack genes for known autotrophic pathways, and have a carbon stable isotope fingerprint heavier than other symbionts from similar habitats. Instead they have the potential to oxidize sulfur to fuel the uptake of organic compounds for heterotrophic growth, a metabolic mode called chemolithoheterotrophy that is not found in other symbioses. Although several symbionts have heterotrophic features to supplement primary production, in Kentron they appear to supplant it entirely.

scholarly journals Horizontal acquisition of a patchwork Calvin cycle by symbiotic and free-living Campylobacterota (formerly Epsilonproteobacteria)

2018 ◽  
Author(s):  
Adrien Assié ◽  
Nikolaus Leisch ◽  
Dimitri V. Meier ◽  
Harald Gruber-Vodicka ◽  
Halina E. Tegetmeyer ◽  
...  
Keyword(s):  
Stable Isotope ◽  
Carbon Fixation ◽  
Tricarboxylic Acid Cycle ◽  
Calvin Cycle ◽  
Tricarboxylic Acid ◽  
Multiple Sources ◽  
Free Living ◽  
Sulfur Oxidizing ◽  
Reductive Tricarboxylic Acid Cycle ◽  
Horizontal Acquisition

AbstractAlthough the majority of known autotrophs use the Calvin-Benson-Bassham (CBB) cycle for carbon fixation, all currently described autotrophs from the Campylobacterota (previously Epsilonproteobacteria) use the reductive tricarboxylic acid cycle (rTCA) instead. We discovered campylobacterotal epibionts (“Candidatus Thiobarba”) of deep-sea mussels that have acquired a complete CBB cycle and lost key genes of the rTCA cycle. Intriguingly, the phylogenies of campylobacterotal CBB genes suggest they were acquired in multiple transfers from Gammaproteobacteria closely related to sulfur-oxidizing endosymbionts associated with the mussels, as well as from Betaproteobacteria. We hypothesize that “Ca. Thiobarba” switched from the rTCA to a fully functional CBB cycle during its evolution, by acquiring genes from multiple sources, including co-occurring symbionts. We also found key CBB cycle genes in free-living Campylobacterota, suggesting that the CBB cycle may be more widespread in this phylum than previously known. Metatranscriptomics and metaproteomics confirmed high expression of CBB cycle genes in mussel-associated “Ca. Thiobarba”. Direct stable isotope fingerprinting showed that “Ca. Thiobarba” has typical CBB signatures, additional evidence that it uses this cycle for carbon fixation. Our discovery calls into question current assumptions about the distribution of carbon fixation pathways across the tree of life, and the interpretation of stable isotope measurements in the environment.

scholarly journals Horizontal acquisition of a patchwork Calvin cycle by symbiotic and free-living Campylobacterota (formerly Epsilonproteobacteria)

2019 ◽  
Vol 14 (1) ◽  
pp. 104-122 ◽  
Author(s):  
Adrien Assié ◽  
Nikolaus Leisch ◽  
Dimitri V. Meier ◽  
Harald Gruber-Vodicka ◽  
Halina E. Tegetmeyer ◽  
...  
Keyword(s):  
Stable Isotope ◽  
Carbon Fixation ◽  
Tricarboxylic Acid Cycle ◽  
Calvin Cycle ◽  
Tricarboxylic Acid ◽  
Multiple Sources ◽  
Free Living ◽  
Sulfur Oxidizing ◽  
Reductive Tricarboxylic Acid Cycle ◽  
Horizontal Acquisition

Abstract Most autotrophs use the Calvin–Benson–Bassham (CBB) cycle for carbon fixation. In contrast, all currently described autotrophs from the Campylobacterota (previously Epsilonproteobacteria) use the reductive tricarboxylic acid cycle (rTCA) instead. We discovered campylobacterotal epibionts (“Candidatus Thiobarba”) of deep-sea mussels that have acquired a complete CBB cycle and may have lost most key genes of the rTCA cycle. Intriguingly, the phylogenies of campylobacterotal CBB cycle genes suggest they were acquired in multiple transfers from Gammaproteobacteria closely related to sulfur-oxidizing endosymbionts associated with the mussels, as well as from Betaproteobacteria. We hypothesize that “Ca. Thiobarba” switched from the rTCA cycle to a fully functional CBB cycle during its evolution, by acquiring genes from multiple sources, including co-occurring symbionts. We also found key CBB cycle genes in free-living Campylobacterota, suggesting that the CBB cycle may be more widespread in this phylum than previously known. Metatranscriptomics and metaproteomics confirmed high expression of CBB cycle genes in mussel-associated “Ca. Thiobarba”. Direct stable isotope fingerprinting showed that “Ca. Thiobarba” has typical CBB signatures, suggesting that it uses this cycle for carbon fixation. Our discovery calls into question current assumptions about the distribution of carbon fixation pathways in microbial lineages, and the interpretation of stable isotope measurements in the environment.

scholarly journals The benthos: the ocean’s last boundary?

2020 ◽  
Vol 84 (4) ◽  
pp. 463-475
Author(s):  
Josep-Maria Gili ◽  
Begoña Vendrell-Simón ◽  
Wolf Arntz ◽  
Francesc Sabater ◽  
Joandomènec Ros
Keyword(s):  
Water Column ◽  
Residence Time ◽  
Food Source ◽  
Benthic Communities ◽  
Strong Impact ◽  
Benthic Organisms ◽  
Main Food ◽  
Sinking Particles ◽  
Main Food Source

Benthic communities depend on receiving much of their food from the water column. While sinking, particles are transformed in a discontinuous process and are temporally retained in transitional physical structures, which act as boundaries and contribute to their further transformation. Motile organisms are well-acquainted with boundaries. The number, width and placement of boundaries are related to the degree of particle degradation or transformation. Progressively deepening within each boundary, particles are degraded according to their residence time in the discontinuity and the activity of the organisms temporarily inhabiting that boundary. Finally, particles reach the seafloor and represent the main food source for benthic organisms; the quality and quantity of this food have a strong impact on the development of benthic communities. However, benthic communities not only play the role of a sink of matter: they act as an active boundary comparable to other oceanic boundaries, in accordance with the boundary concept proposed by the ecologist Ramon Margalef.

scholarly journals Carbon Assimilation Strategies in Ultrabasic Groundwater: Clues from the Integrated Study of a Serpentinization-Influenced Aquifer

mSystems ◽  
2020 ◽  
Vol 5 (2) ◽  
Author(s):  
Lauren M. Seyler ◽  
William J. Brazelton ◽  
Craig McLean ◽  
Lindsay I. Putman ◽  
Alex Hyer ◽  
...  
Keyword(s):  
Microbial Communities ◽  
Carbon Fixation ◽  
Dissolved Inorganic Carbon ◽  
Sequence Data ◽  
Tricarboxylic Acid Cycle ◽  
Carbon Sources ◽  
Mass Spectrometry Data ◽  
Physiological Adaptation ◽  
Coast Range ◽  
Coast Range Ophiolite

ABSTRACT Serpentinization is a low-temperature metamorphic process by which ultramafic rock chemically reacts with water. Such reactions provide energy and materials that may be harnessed by chemosynthetic microbial communities at hydrothermal springs and in the subsurface. However, the biogeochemistry mediated by microbial populations that inhabit these environments is understudied and complicated by overlapping biotic and abiotic processes. We applied metagenomics, metatranscriptomics, and untargeted metabolomics techniques to environmental samples taken from the Coast Range Ophiolite Microbial Observatory (CROMO), a subsurface observatory consisting of 12 wells drilled into the ultramafic and serpentinite mélange of the Coast Range Ophiolite in California. Using a combination of DNA and RNA sequence data and mass spectrometry data, we found evidence for several carbon fixation and assimilation strategies, including the Calvin-Benson-Bassham cycle, the reverse tricarboxylic acid cycle, the reductive acetyl coenzyme A (acetyl-CoA) pathway, and methylotrophy, in the microbial communities inhabiting the serpentinite-hosted aquifer. Our data also suggest that the microbial inhabitants of CROMO use products of the serpentinization process, including methane and formate, as carbon sources in a hyperalkaline environment where dissolved inorganic carbon is unavailable. IMPORTANCE This study describes the potential metabolic pathways by which microbial communities in a serpentinite-influenced aquifer may produce biomass from the products of serpentinization. Serpentinization is a widespread geochemical process, taking place over large regions of the seafloor and at continental margins, where ancient seafloor has accreted onto the continents. Because of the difficulty in delineating abiotic and biotic processes in these environments, major questions remain related to microbial contributions to the carbon cycle and physiological adaptation to serpentinite habitats. This research explores multiple mechanisms of carbon fixation and assimilation in serpentinite-hosted microbial communities.

scholarly journals The effect of abiotic and biotic factors on the importance of macroplankton in the diet of Northeast Arctic cod in recent years

2005 ◽  
Vol 62 (7) ◽  
pp. 1463-1474 ◽  
Author(s):  
E.L. Orlova ◽  
A.V. Dolgov ◽  
G.B. Rudneva ◽  
V.N. Nesterova
Keyword(s):  
Energy Balance ◽  
Food Source ◽  
Water Mass ◽  
Ecological Groups ◽  
Biotic Factors ◽  
Low Fat ◽  
Main Food ◽  
Different Types ◽  
Abiotic And Biotic Factors ◽  
Main Food Source

AbstractUsing cod feeding data, this paper considers the distribution and abundance of macroplankton from different ecological groups (euphausiids and hyperiids) and the variability in their consumption by cod over a period of years during which different water mass temperatures were observed. These years were also characterized by variable abundance of capelin, cod's main food source. Differences in intensity and duration of cod consumption of euphausiids and hyperiids species are shown, depending on their abundance, temperature conditions, cod distribution, and the supply of capelin for cod. This paper discusses the energetics of consuming different types of prey and the role euphausiids play in the energy balance of cod. The low fat content of cod is sometimes associated with feeding on postspawning euphausiids in summer and autumn.

A preliminary investigation of the lipids and fatty acids composition of Gammarus aequicauda (Crustacea: Amphipoda) and its main food source

2006 ◽  
Vol 86 (2) ◽  
pp. 345-348 ◽  
Author(s):  
Francesca Biandolino ◽  
Ermelinda Prato
Keyword(s):  
Fatty Acids ◽  
Food Source ◽  
Unsaturated Fatty Acids ◽  
Southern Italy ◽  
Preliminary Investigation ◽  
Monounsaturated Fatty Acids ◽  
Main Food ◽  
Gammarus Aequicauda ◽  
Chaetomorpha Linum ◽  
Main Food Source

Lipid and fatty acid composition in Gammarus aequicauda from Mar Piccolo (Ionian Sea, southern Italy) were studied during the spring months. Simultaneously, samples of the macroalgae Chaetomorpha linum were also collected from the same area. During these months Chaetomorpha linum was the main food source of Gammarus aequicauda. The main lipid classes were phospholipids (PL) and triacylglycerols (TG) both in Gammarus aequicauda and in Chaetomorpha linum with similar concentrations. But PL was the main lipid class in Gammarus aequicauda and TG in Chaetomorpha linum. On average unsaturated fatty acids represent the preponderant part in both G. aequicauda and C. linum. Gammarus aequicauda had a higher level in monounsaturated fatty acids (MUFA), on the contrary polyunsaturated fatty acids (PUFA) were the dominant unsaturated fatty acids in C. linum. Both were characterized by high levels of 18:0, 18:1(n-9), 20:5(n-3) and 20:4(n-6), in particular C. linum had a high proportion of 14:0 and the ratio of 18:1n 9/18:1n 7 was high.

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