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 ◽  
...  

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.

mBio ◽  
2019 ◽  
Vol 10 (3) ◽  
Author(s):  
Brandon K. B. Seah ◽  
Chakkiath Paul Antony ◽  
Bruno Huettel ◽  
Jan Zarzycki ◽  
Lennart Schada von Borzyskowski ◽  
...  

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.


2020 ◽  
Vol 84 (4) ◽  
pp. 463-475
Author(s):  
Josep-Maria Gili ◽  
Begoña Vendrell-Simón ◽  
Wolf Arntz ◽  
Francesc Sabater ◽  
Joandomènec Ros

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.


2005 ◽  
Vol 62 (7) ◽  
pp. 1463-1474 ◽  
Author(s):  
E.L. Orlova ◽  
A.V. Dolgov ◽  
G.B. Rudneva ◽  
V.N. Nesterova

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.


Author(s):  
Francesca Biandolino ◽  
Ermelinda Prato

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.


2015 ◽  
Vol 17 (1) ◽  
pp. 170 ◽  
Author(s):  
A. TERRÓN-SIGLERA ◽  
D. LEÓN-MUEZ ◽  
P. PEÑALVER-DUQUE ◽  
F. ESPINOSA TORRE

The endangered and Mediterranean endemic orange coral (Astroides calycularis) hosts an important macrofaunal assemblage. The gut contents of the main peracarids associated with the orange coral were analysed. In total 161 specimens belonging to 11 species and 9 families were examined on the southern coast of the Iberian Peninsula. The gut content study was carried out introducing the specimens of each species in Hertwig’s liquid. The analysis revealed that the peracarid species associated with A. calycularis had different feeding strategies and their main food source was detritus. The results highlight that peracarids may depend on the host and the detritus that the coral produces.


2019 ◽  
Vol 78 (3) ◽  
Author(s):  
Elisa A. C. C. Alvim ◽  
Tiago B. Kisaka ◽  
Gabriela B. Nardoto ◽  
Luciana De Mendonça-Galvão ◽  
Barbara M. Fonseca ◽  
...  

Ponds arising from groundwater in Cerrado of Central Brazil are oligotrophic but highly biodiverse environments. In this study, we used stable isotope ratios to test if there are variations in carbon and nitrogen acquisition by different primary food sources and if they are influenced by seasonality in a well-preserved pond. We hypothesized that periphyton is the main food source for macrophyte-associated fauna. We found that δ13C, but not δ15N, can distinguish between primary food sources; however, the isotopic signatures of food sources did not differ significantly between seasons. The δ15N values of macrophyte-associated fauna were significantly higher for predators compared with other trophic groups, but δ13C values did not differ significantly between groups. Emergent macrophytes and periphyton were the main food sources for scrapers (contribution of 42.5%) and collector-gatherers (contribution of 41.6%), respectively. Compared with emergent macrophytes, submerged macrophytes were associated with a greater abundance of fauna and algal biomass but were not a significant food source for associated fauna. Our findings demonstrate that in this small shallow oligotrophic pond in the Cerrado, the stable isotope ratios of carbon and nitrogen of food sources did not vary between seasons but did differ between aquatic macrophyte life forms. We point out the different functional roles of macrophyte life forms, with emergent macrophytes serving as an important food resource, while submerged macrophytes mainly provide physical structure.


2018 ◽  
Author(s):  
Adrien Assié ◽  
Nikolaus Leisch ◽  
Dimitri V. Meier ◽  
Harald Gruber-Vodicka ◽  
Halina E. Tegetmeyer ◽  
...  

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.


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