scholarly journals Anaerobic sulfur oxidation underlies adaptation of a chemosynthetic symbiont to oxic-anoxic interfaces

2020 ◽  
Author(s):  
Gabriela F. Paredes ◽  
Tobias Viehboeck ◽  
Raymond Lee ◽  
Marton Palatinszky ◽  
Michaela A. Mausz ◽  
...  

AbstractChemosynthetic symbioses occur worldwide in marine habitats. However, physiological studies of chemoautotrophic bacteria thriving on animals are scarce. Stilbonematinae are coated by monocultures of thiotrophic Gammaproteobacteria. As these nematodes migrate through the redox zone, their ectosymbionts experience varying oxygen concentrations. Here, by applying omics, Raman microspectroscopy and stable isotope labeling, we investigated the effect of oxygen on the metabolism of Candidatus Thiosymbion oneisti. Unexpectedly, sulfur oxidation genes were upregulated in anoxic relative to oxic conditions, but carbon fixation genes and incorporation of 13C-labeled bicarbonate were not. Instead, several genes involved in carbon fixation, the assimilation of organic carbon and polyhydroxyalkanoate (PHA) biosynthesis, as well as nitrogen fixation and urea utilization were upregulated in oxic conditions. Furthermore, in the presence of oxygen, stress-related genes were upregulated together with vitamin and cofactor biosynthesis genes likely necessary to withstand its deleterious effects.Based on this first global physiological study of a chemosynthetic ectosymbiont, we propose that, in anoxic sediment, it proliferates by utilizing nitrate to oxidize reduced sulfur, whereas in superficial sediment it exploits aerobic respiration to facilitate assimilation of carbon and nitrogen to survive oxidative stress. Both anaerobic sulfur oxidation and its decoupling from carbon fixation represent unprecedented adaptations among chemosynthetic symbionts.

2016 ◽  
Vol 167 (5) ◽  
pp. 357-366 ◽  
Author(s):  
Jiri Kucera ◽  
Eva Pakostova ◽  
Jan Lochman ◽  
Oldrich Janiczek ◽  
Martin Mandl

Microbiome ◽  
2021 ◽  
Vol 9 (1) ◽  
Author(s):  
Marie-Anne Cambon-Bonavita ◽  
Johanne Aubé ◽  
Valérie Cueff-Gauchard ◽  
Julie Reveillaud

Abstract Background Free-living and symbiotic chemosynthetic microbial communities support primary production and higher trophic levels in deep-sea hydrothermal vents. The shrimp Rimicaris exoculata, which dominates animal communities along the Mid-Atlantic Ridge, houses a complex bacterial community in its enlarged cephalothorax. The dominant bacteria present are from the taxonomic groups Campylobacteria, Desulfobulbia (formerly Deltaproteobacteria), Alphaproteobacteria, Gammaproteobacteria, and some recently discovered iron oxyhydroxide-coated Zetaproteobacteria. This epibiotic consortium uses iron, sulfide, methane, and hydrogen as energy sources. Here, we generated shotgun metagenomes from Rimicaris exoculata cephalothoracic epibiotic communities to reconstruct and investigate symbiotic genomes. We collected specimens from three geochemically contrasted vent fields, TAG, Rainbow, and Snake Pit, to unravel the specificity, variability, and adaptation of Rimicaris–microbe associations. Results Our data enabled us to reconstruct 49 metagenome-assembled genomes (MAGs) from the TAG and Rainbow vent fields, including 16 with more than 90% completion and less than 5% contamination based on single copy core genes. These MAGs belonged to the dominant Campylobacteria, Desulfobulbia, Thiotrichaceae, and some novel candidate phyla radiation (CPR) lineages. In addition, most importantly, two MAGs in our collection were affiliated to Zetaproteobacteria and had no close relatives (average nucleotide identity ANI < 77% with the closest relative Ghiorsea bivora isolated from TAG, and 88% with each other), suggesting potential novel species. Genes for Calvin-Benson Bassham (CBB) carbon fixation, iron, and sulfur oxidation, as well as nitrate reduction, occurred in both MAGs. However, genes for hydrogen oxidation and multicopper oxidases occurred in one MAG only, suggesting shared and specific potential functions for these two novel Zetaproteobacteria symbiotic lineages. Overall, we observed highly similar symbionts co-existing in a single shrimp at both the basaltic TAG and ultramafic Rainbow vent sites. Nevertheless, further examination of the seeming functional redundancy among these epibionts revealed important differences. Conclusion These data highlight microniche partitioning in the Rimicaris holobiont and support recent studies showing that functional diversity enables multiple symbiont strains to coexist in animals colonizing hydrothermal vents.


2021 ◽  
Vol 8 ◽  
Author(s):  
Michael Lintner ◽  
Bianca Lintner ◽  
Wolfgang Wanek ◽  
Sarina Schmidt ◽  
Nina Keul ◽  
...  

Marine carbon and nitrogen processing through microorganisms’ metabolism is an important aspect of the global element cycles. For that purpose, we used foraminifera to analyze the element turnover with different algae food sources. In the Baltic Sea, benthic foraminifera are quite common and therefore it is important to understand their metabolism. Especially, Cribroelphidium selseyense, also occurring in the Baltic Sea, has often been used for laboratory feeding experiments to test their effect on carbon or nitrogen turnover. Therefore, foraminifera were collected from the Kiel Fjord and fed with six different algal species in two qualities (freeze-dried algae vs. fresh algae, all 13C- and 15N-labeled). Also, labeled dissolved inorganic C and N compounds and glucose were offered to the foraminifera to test direct assimilation of dissolved compounds (carbon and nitrogen) from the water column. Our experiments showed that after 15 days of incubation, there were highly significant differences in isotope labeling in foraminifera fed with fresh algae and dry algae, depending on algal species. Further, different algal species led to different 13C and 15N enrichment in the studied foraminifera, highlighting a feeding preference for one diatom species and an Eustigmatophyte. A significant carbon assimilation from HCO3– was observed after 7 days of incubation. The N assimilation from NH4+ was significantly higher than for NO3– as an inorganic N source. The uptake of glucose showed a lag phase, which was often observed during past experiments, where foraminifera were in a steady state and showed no food uptake at regular intervals. These results highlight the importance of food quality on the feeding behavior and metabolic pathways for further studies of foraminiferal nutrition and nutrient cycling.


2019 ◽  
Vol 85 (24) ◽  
Author(s):  
Cameron M. Callbeck ◽  
Chris Pelzer ◽  
Gaute Lavik ◽  
Timothy G. Ferdelman ◽  
Jon S. Graf ◽  
...  

ABSTRACT Members of the epsilonproteobacterial genus Arcobacter have been identified to be potentially important sulfide oxidizers in marine coastal, seep, and stratified basin environments. In the highly productive upwelling waters off the coast of Peru, Arcobacter cells comprised 3 to 25% of the total microbial community at a near-shore station where sulfide concentrations exceeded 20 μM in bottom waters. From the chemocline where the Arcobacter population exceeded 106 cells ml−1 and where high rates of denitrification (up to 6.5 ± 0.4 μM N day−1) and dark carbon fixation (2.8 ± 0.2 μM C day−1) were measured, we isolated a previously uncultivated Arcobacter species, Arcobacter peruensis sp. nov. (BCCM LMG-31510). Genomic analysis showed that A. peruensis possesses genes encoding sulfide oxidation and denitrification pathways but lacks the ability to fix CO2 via autotrophic carbon fixation pathways. Genes encoding transporters for organic carbon compounds, however, were present in the A. peruensis genome. Physiological experiments demonstrated that A. peruensis grew best on a mix of sulfide, nitrate, and acetate. Isotope labeling experiments further verified that A. peruensis completely reduced nitrate to N2 and assimilated acetate but did not fix CO2, thus coupling heterotrophic growth to sulfide oxidation and denitrification. Single-cell nanoscale secondary ion mass spectrometry analysis of samples taken from shipboard isotope labeling experiments also confirmed that the Arcobacter population in situ did not substantially fix CO2. The efficient growth yield associated with the chemolithoheterotrophic metabolism of A. peruensis may allow this Arcobacter species to rapidly bloom in eutrophic and sulfide-rich waters off the coast of Peru. IMPORTANCE Our multidisciplinary approach provides new insights into the ecophysiology of a newly isolated environmental Arcobacter species, as well as the physiological flexibility within the Arcobacter genus and sulfide-oxidizing, denitrifying microbial communities within oceanic oxygen minimum zones (OMZs). The chemolithoheterotrophic species Arcobacter peruensis may play a substantial role in the diverse consortium of bacteria that is capable of coupling denitrification and fixed nitrogen loss to sulfide oxidation in eutrophic, sulfidic coastal waters. With increasing anthropogenic pressures on coastal regions, e.g., eutrophication and deoxygenation (D. Breitburg, L. A. Levin, A. Oschlies, M. Grégoire, et al., Science 359:eaam7240, 2018, https://doi.org/10.1126/science.aam7240), niches where sulfide-oxidizing, denitrifying heterotrophs such as A. peruensis thrive are likely to expand.


2000 ◽  
Vol 27 (6) ◽  
pp. 507 ◽  
Author(s):  
Charlotte E. Lewis ◽  
Graham Noctor ◽  
David Causton ◽  
Christine H. Foyer

Concepts of the regulation of assimilate partitioning in leaves frequently consider only the allocation of carbon between sucrose and starch synthesis, storage and export. While carbohydrate metabolism accounts for a large proportion of assimilated carbon, such analyses provide only a restricted view of carbon metabolism and partitioning in leaf cells since photosynthetic carbon fixation provides precursors for all other biosynthetic pathways in the plant. Most of these precursors are required for biosynthesis of amino acids that form the building blocks for many compounds in plants. We have used leaf carbon : nitrogen ratios to calculate the allocation of photosynthetic electrons to the assimilation of nitrogen necessary for amino acid formation, and conclude that this allocation is variable but may be higher than values often quoted in the literature. Respiration is a significant fate of fixed carbon. In addition to supplying biosynthetic precursors, respiration is required for energy production and may also act, in both light and dark, to balance cellular energy budgets. We have used growth CO2 concentration and irradiance to modify source activity in Lolium temulentum in order to explore the interactions between photosynthetic carbon and nitrogen assimilation, assimilate production, respiration and export. It is demonstrated that there is a robust correlation between source activity and foliar respiration rates. Under some conditions concomitant increases in source activity and respiration may be necessary to support faster growth. In other conditions, increases in respiration appear to result from internal homeostatic mechanisms that may be candidate targets for increasing yield.


2010 ◽  
Vol 13 (3) ◽  
pp. 758-774 ◽  
Author(s):  
Sabine Lenk ◽  
Julia Arnds ◽  
Katrice Zerjatke ◽  
Niculina Musat ◽  
Rudolf Amann ◽  
...  

2006 ◽  
Vol 73 (4) ◽  
pp. 1174-1179 ◽  
Author(s):  
Kathleen M. Scott ◽  
Colleen M. Cavanaugh

ABSTRACT Chemoautotrophic symbioses, in which endosymbiotic bacteria are the major source of organic carbon for the host, are found in marine habitats where sulfide and oxygen coexist. The purpose of this study was to determine the influence of pH, alternate sulfur sources, and electron acceptors on carbon fixation and to investigate which form(s) of inorganic carbon is taken up and fixed by the gamma-proteobacterial endosymbionts of the protobranch bivalve Solemya velum. Symbiont-enriched suspensions were generated by homogenization of S. velum gills, followed by velocity centrifugation to pellet the symbiont cells. Carbon fixation was measured by incubating the cells with 14C-labeled dissolved inorganic carbon. When oxygen was present, both sulfide and thiosulfate stimulated carbon fixation; however, elevated levels of either sulfide (>0.5 mM) or oxygen (1 mM) were inhibitory. In the absence of oxygen, nitrate did not enhance carbon fixation rates when sulfide was present. Symbionts fixed carbon most rapidly between pH 7.5 and 8.5. Under optimal pH, sulfide, and oxygen conditions, symbiont carbon fixation rates correlated with the concentrations of extracellular CO2 and not with HCO3 − concentrations. The half-saturation constant for carbon fixation with respect to extracellular dissolved CO2 was 28 � 3 μM, and the average maximal velocity was 50.8 � 7.1 μmol min−1 g of protein−1. The reliance of S. velum symbionts on extracellular CO2 is consistent with their intracellular lifestyle, since HCO3 − utilization would require protein-mediated transport across the bacteriocyte membrane, perisymbiont vacuole membrane, and symbiont outer and inner membranes. The use of CO2 may be a general trait shared with many symbioses with an intracellular chemoautotrophic partner.


2018 ◽  
Vol 15 (18) ◽  
pp. 5503-5517 ◽  
Author(s):  
P. Sadanandan Bhavya ◽  
Jang Han Lee ◽  
Ho Won Lee ◽  
Jae Joong Kang ◽  
Jae Hyung Lee ◽  
...  

Abstract. Carbon and nitrogen uptake rates by small phytoplankton (0.7–5 µm) in the Kara, Laptev, and East Siberian seas in the Arctic Ocean were quantified using in situ isotope labeling experiments; this research, which was novel and part of the NABOS (Nansen and Amundsen Basins Observational System) program, took place from 21 August to 22 September 2013. The depth-integrated carbon (C), nitrate (NO3-), and ammonium (NH4+) uptake rates by small phytoplankton ranged from 0.54 to 15.96 mg C m−2 h−1, 0.05 to 1.02 mg C m−2 h−1, and 0.11 to 3.73 mg N m−2 h−1, respectively. The contributions of small phytoplankton towards the total C, NO3-, and NH4+ varied from 25 % to 89 %, 31 % to 89 %, and 28 % to 91 %, respectively. The turnover times for NO3- and NH4+ by small phytoplankton found in the present study indicate the longer residence times (years) of the nutrients in the deeper waters, particularly for NO3-. Additionally, the relatively higher C and N uptake rates by small phytoplankton obtained in the present study from locations with less sea ice concentration indicate the possibility that small phytoplankton thrive under the retreat of sea ice as a result of warming conditions. The high contributions of small phytoplankton to the total C and N uptake rates suggest the capability of small autotrophs to withstand the adverse hydrographic conditions introduced by climate change.


2021 ◽  
Author(s):  
Nanqing Zhou ◽  
Jessica L. Keffer ◽  
Shawn W. Polson ◽  
Clara S Chan

Sideroxydans lithotrophicus ES-1 grows autotrophically either by Fe(II) oxidation or thiosulfate oxidation, in contrast to most other neutrophilic Fe(II)-oxidizing bacteria (FeOB) isolates. This provides a unique opportunity to explore the physiology of a facultative FeOB and constrain the genes specific to Fe(II) oxidation. We compared the growth of S. lithotrophicus ES-1 on Fe(II), thiosulfate, and both substrates together. While initial growth rates were similar, thiosulfate-grown cultures had higher yield with or without Fe(II) present, which may give ES-1 an advantage over obligate FeOB. To investigate the Fe(II) and S oxidation pathways, we conducted transcriptomics experiments, validated with RT-qPCR. We explored the long-term gene expression response at different growth phases (over days-week) and expression changes during a short-term switch from thiosulfate to Fe(II) (90 min). The dsr and sox sulfur oxidation genes were upregulated in thiosulfate cultures. The Fe(II) oxidase gene cyc2 was among the top expressed genes during both Fe(II) and thiosulfate oxidation, and addition of Fe(II) to thiosulfate-grown cells caused an increase in cyc2 expression. These results support the role of Cyc2 as the Fe(II) oxidase and suggest that ES-1 maintains readiness to oxidize Fe(II) even in the absence of Fe(II). We used gene expression profiles to further constrain the ES-1 Fe(II) oxidation pathway. Notably, among the most highly upregulated genes during Fe(II) oxidation were genes for alternative complex III, reverse electron transport and carbon fixation. This implies a direct connection between Fe(II) oxidation and carbon fixation, suggesting that CO2 is an important electron sink for Fe(II) oxidation.


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