Sulfate is transported at significant rates through the symbiosome membrane and is crucial for nitrogenase biosynthesis

Schneider, Sebastian; Schintlmeister, Arno; Becana, Manuel; Wagner, Michael; Woebken, Dagmar; Wienkoop, Stefanie

doi:10.1111/pce.13481

Cited by 35 publications

(17 citation statements)

References 62 publications

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“…Indeed, despite the sensitivity of nitrogenase toward oxygen (81), its key catalytic MoFe enzymes (nifD, nifK; 82) and several other genes involved in nitrogen fixation were drastically upregulated in the presence of oxygen (Figures 1 and 3). Moreover, in accordance with a recent study showing the importance of sulfur assimilation for nitrogen fixation (83), genes involved in the assimilation of sulfate, i.e. the sulfate transporters sulP and cysZ as well as genes encoding two enzymes responsible for cysteine biosynthesis (cysM, cysE) were also upregulated in the presence of oxygen (Data S1).…”

Section: Upregulation Of Nitrogen Assimilation In the Presence Of Oxygensupporting

confidence: 90%

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

Paredes

Viehboeck

Lee

et al. 2020

Preprint

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57Chemosynthetic symbioses occur worldwide in marine habitats. However, physiological 58 studies of chemoautotrophic bacteria thriving on animals are scarce. Stilbonematinae are 59 coated by monocultures of thiotrophic Gammaproteobacteria. As these nematodes migrate 60 through the redox zone, their ectosymbionts experience varying oxygen concentrations. 61Here, by applying omics, Raman microspectroscopy and stable isotope labeling, we 62 investigated the effect of oxygen on the metabolism of Candidatus Thiosymbion oneisti. 63Unexpectedly, sulfur oxidation genes were upregulated in anoxic relative to oxic conditions, 64 but carbon fixation genes and incorporation of 13 C-labeled bicarbonate were not. Instead, 65several genes involved in carbon fixation, the assimilation of organic carbon and 66 polyhydroxyalkanoate (PHA) biosynthesis, as well as nitrogen fixation and urea utilization 67 were upregulated in oxic conditions. Furthermore, in the presence of oxygen, stress-related 68 genes were upregulated together with vitamin and cofactor biosynthesis genes likely 69 necessary to withstand its deleterious effects. 70Based on this first global physiological study of a chemosynthetic ectosymbiont, we 71propose that, in anoxic sediment, it proliferates by utilizing nitrate to oxidize reduced sulfur, 72whereas in superficial sediment it exploits aerobic respiration to facilitate assimilation of 73 carbon and nitrogen to survive oxidative stress. Both anaerobic sulfur oxidation and its 74 decoupling from carbon fixation represent unprecedented adaptations among 75 chemosynthetic symbionts. 76 77 intracorporeal thiotrophic bacteria, it is generally accepted that the endosymbiont's 85 chemosynthetic metabolism serves to provide organic carbon for feeding the animal host 86[reviewed in 1-3]. In addition, some chemosynthetic symbionts have been found capable to 87 fix atmospheric nitrogen, albeit symbiont-to-host transfer of fixed nitrogen remains unproven 88 [4, 5]. As for the rarer chemosynthetic bacterial-animal associations in which symbionts 89 colonize exterior surfaces (ectosymbionts), fixation of inorganic carbon and transfer of 90 organic carbon to the host has only been demonstrated for the microbial community 91 colonizing the gill chamber of the hydrothermal vent shrimp Rimicaris exoculata [6]. 92In this study, we focused on Candidatus Thiosymbion oneisti, a 93Gammaproteobacterium belonging to the basal family of Chromatiaceae (also known as 94 purple sulfur bacteria), which colonizes the surface of the marine nematode Laxus oneistus 95 (Stilbonematinae). Curiously, this group of free-living roundworms represents the only known 96 animals engaging in monospecific ectosymbioses, i.e. each nematode species is 97 ensheathed by a single Ca. Thiosymbion phylotype, and, in the case of Ca. T. oneisti, the 98 bacteria form a single layer on the cuticle of its host [7-11]. Moreover, the rod-shaped 99 representatives of this bacterial genus, including Ca. T. oneisti, divide by FtsZ-based 100 longitudinal fission, a unique ...

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Section: Upregulation Of Nitrogen Assimilation In the Presence Of Oxygensupporting

confidence: 90%

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

Paredes

Viehboeck

Lee

et al. 2020

Preprint

Self Cite

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“…In addition, S nutrition also affects N fixation in legumes. For example, the application of S fertilizers could increase the capacity of N fixation in peas ( Pisum sativum L.) and alfalfa ( Medicago sativa L.) [ 20 , 21 ].…”

Section: The Physiological Functions Of S In Plantsmentioning

confidence: 99%

Sulfur Homeostasis in Plants

Gao

Yang

2020

IJMS

113

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Sulfur (S) is an essential macronutrient for plant growth and development. S is majorly absorbed as sulfate from soil, and is then translocated to plastids in leaves, where it is assimilated into organic products. Cysteine (Cys) is the first organic product generated from S, and it is used as a precursor to synthesize many S-containing metabolites with important biological functions, such as glutathione (GSH) and methionine (Met). The reduction of sulfate takes place in a two-step reaction involving a variety of enzymes. Sulfate transporters (SULTRs) are responsible for the absorption of SO42− from the soil and the transport of SO42− in plants. There are 12–16 members in the S transporter family, which is divided into five categories based on coding sequence homology and biochemical functions. When exposed to S deficiency, plants will alter a series of morphological and physiological processes. Adaptive strategies, including cis-acting elements, transcription factors, non-coding microRNAs, and phytohormones, have evolved in plants to respond to S deficiency. In addition, there is crosstalk between S and other nutrients in plants. In this review, we summarize the recent progress in understanding the mechanisms underlying S homeostasis in plants.

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“…Availability of fixed nitrogen forms in soils inhibits nodulation (Streeter, 1987). Similarly, low levels of photosynthates, phosphate, or sulphate transfer from the host plant decrease nodulation and nitrogen fixation rates (Singleton and van Kessel, 1987;Valentine et al, 2017;Schneider et al, 2019). Transition metals such as iron, copper, zinc, or molybdenum are also critical for nodulation and nitrogen fixation as cofactors in many of the involved enzymes (González-Guerrero et al, 2014;González-Guerrero et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Nicotianamine Synthase 2 Is Required for Symbiotic Nitrogen Fixation in Medicago truncatula Nodules

et al. 2020

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Symbiotic nitrogen fixation carried out by the interaction between legumes and diazotrophic bacteria known as rhizobia requires relatively large levels of transition metals. These elements are cofactors of many key enzymes involved in this process. Metallic micronutrients are obtained from soil by the roots and directed to sink organs by the vasculature, in a process mediated by a number of metal transporters and small organic molecules that facilitate metal delivery in the plant fluids. Among the later, nicotianamine is one of the most important. Synthesized by nicotianamine synthases (NAS), this molecule forms metal complexes participating in intracellular metal homeostasis and long-distance metal trafficking. Here we characterized the NAS2 gene from model legume Medicago truncatula. MtNAS2 is located in the root vasculature and in all nodule tissues in the infection and fixation zones. Symbiotic nitrogen fixation requires of MtNAS2 function, as indicated by the loss of nitrogenase activity in the insertional mutant nas2-1, phenotype reverted by reintroduction of a wild-type copy of MtNAS2. This would result from the altered iron distribution in nas2-1 nodules shown with X-ray fluorescence. Moreover, iron speciation is also affected in these nodules. These data suggest a role of nicotianamine in iron delivery for symbiotic nitrogen fixation.

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Sulfate is transported at significant rates through the symbiosome membrane and is crucial for nitrogenase biosynthesis

Cited by 35 publications

References 62 publications

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

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

Sulfur Homeostasis in Plants

Nicotianamine Synthase 2 Is Required for Symbiotic Nitrogen Fixation in Medicago truncatula Nodules

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