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Enzyme adaptation to habitat thermal legacy shapes the thermal plasticity of marine microbiomes

ABSTRACT: Microbial communities respond to temperature with physiological adaptation and compositional turnover. Whether thermal selection of enzymes explains marine microbiome plasticity in response to temperature remains unresolved. By quantifying the thermal behaviour of seven functionally-independent enzyme classes (esterase, extradiol dioxygenase, phosphatase, beta-galactosidase, nuclease, transaminase, and aldo-keto reductase) in native proteomes of marine sediment microbiomes from the Irish Sea to the southern Red Sea, we record a significant effect of the mean annual temperature (MAT) on enzyme’s response (R2, 0.51–0.80, p < 0.01 in all cases). Activity and stability profiles of 228 esterases and 5 extradiol dioxygenases from sediment and seawater across 70 locations worldwide (latitude 62.2°S–16°N, MAT –1.4ºC–29.5ºC) validate this thermal pattern. Modelling the esterase phase transition temperature as a measure of structural flexibility, confirm the observed relationship with MAT. Furthermore, when considering temperature variability in sites with non-significantly different MATs, the broadest range of enzyme thermal behaviour and the highest growth plasticity of the enriched heterotrophic bacteria occur in samples with the widest annual thermal variability. These results indicate that temperature-driven enzyme selection shapes microbiome thermal plasticity and that thermal variability finely tunes such processes and should be considered alongside MAT in forecasting microbial community thermal response

INSTRUMENT(S): TripleTOF 5600

ORGANISM(S): Eubacteriales

SUBMITTER: Sergio Ciordia

LAB HEAD: Daniele Daffonchio

PROVIDER: PXD039714 | Pride | 2023-02-07

REPOSITORIES: Pride

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Persulfidated subproteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes and nuclear translocation of glyceraldehyde-3-phosphate dehydrogenase in plants.

Project description:Hydrogen sulfide-mediated signaling pathways regulates many physiological andpathophysiological processes in mammalian and plant systems. The molecular mechanism bywhich hydrogen sulfide exerts its action involves the oxidative post-translational modificationof cysteine residues to form a persulfidated thiol motif, named as protein S-sulfhydration orpersulfidation. We have developed a comparative and quantitative proteomic analysisapproach for the detection of endogenous S-sulfhydrated proteins in wild-type Arabidopsisand L-CYSTEINE DESULFHYDRASE 1 mutant leaves by using the tag-switch method.Bioinformatic analysis of the identified proteins revealed that S-sulfhydrated cysteines arepart of a wide range of biological functions regulating important processes such as carbonmetabolism, plant responses to abiotic and biotic stresses, plant growth and development, andRNA translation. Quantitative analysis in both genetic backgrounds reveals hydrogen sulfidemediatedprotein sulfhydration as a new regulatory component in primary metabolic pathwayssuch as tricarboxylic acid cycle, glycolysis or Calvin cycle. In addition, studies on thesubcellular localization of glyceraldehyde-3-phosphate dehydrogenase show that sulfideregulates the cytosolic/nuclear partitioning by enhancing the nuclear localization of theprotein and appears to be a critical step for reprogramming cellular metabolism.

2017-10-27 | PXD005168 | Pride

Differential gene expression in Leishmania [SPP.] promastigotes. Leishmania chagasi

Project description:Leishmania chagasi is the causative agent of zoonotic visceral leishmaniasis in Brazil, being domestic and stray dogs the main reservoirs. The development of the parasite involves two stages. The promastigote is extracellular and develops within the sand fly gut. The amastigote survives inside the harsh environment of the phagolysosome of mammalian host phagocytes, where pH is acidic, temperature higher than in the sand fly vector and hydrolytic enzymes act. In addition, the host phagocyte displays the nitric oxide defense mechanism against the amastigote. Promastigotes are also able to withstand NO even when they develop within the sand fly gut. This can be explained with the pre-adaptative hypothesis, which has been supported by us and others elsewhere and consists of preparation of promastigotes in advance for development towards the amastigote stage. For this reason, the comparison of NO-resistant and sensitive promastigotes is valuable. The two-dimension electrophoresis-mass spectrometry (2DE-MS/MS) approach has been performed to study differential protein abundance comparing L. chagasi NO-sensitive and resistant promastigotes. This analysis has revealed differential expression of genes directly and indirectly involved in NO-resistance, highlighting up-regulation of the glucose-6-phosphate dehydrogenase (G6PD) in NO-resistant promastigotes and down-regulation of the glutathione peroxidase (GPX) and the arginase (ARG) in NO-sensitive ones. These data are a starting point in the search of vaccine candidates and/or drug targets.

2016-03-31 | PXD002939 | Pride

Detailed map of the Pseudomonas aeruginosa Crc regulon using a new parameter for tracking post-transcriptional regulation

Project description:Bacterial physiology in general and the bacterial response to the presence of nutrients and to external signals in particular is regulated at different levels, from mRNA synthesis to translational regulation and protein modification. However, there are not standardized parameters for defining post-transcriptional regulation. Herein, we propose a simple parameter, dubbed post-transcriptional variation (PTV), that allow extracting information on translational regulation from the combined analysis of transcriptomic and proteomic data. We have applied this parameter for precisely defining the regulon of the Pseudomonas aeruginosa post-transcriptional regulator Crc. P. aeruginosa is a free-living microorganism that, besides colonizing a diversity of environmental habitats, is able to infect a large number of patients at hospitals. Part of the ability of P. aeruginosa for colonizing such a variety of habitats relies on its capability of using a large number of carbon sources. This hierarchical assimilation is regulated by Crc, which together with Hfq, binds its target RNA impeding their translation when catabolite repression is triggered. Most studies cannot provide information on post-transcriptional regulation when analysed independently. Using the defined PTV parameter, we present a comprehensive map of the Crc post-transcriptional regulon.

2018-11-13 | PXD009809 | Pride

The Hypervariable Amino-Terminus of P1 Protease Modulates Potyviral Replication and Host Defense Responses

Project description:The replication of many RNA viruses involves the translation of polyproteins, whose processing by endopeptidases is a critical step for the release of functional subunits. P1 is the first protease encoded in plant potyvirus genomes; once activated by an as-yet-unknown host factor, it acts in cis on its own C-terminal end, hydrolyzing the P1-HCPro junction. Earlier research suggests that P1 cooperates with HCPro to inhibit host RNA silencing defenses. Using Plum pox virus as a model, we show that although P1 does not have a major direct role in RNA silencing suppression, it can indeed modulate HCPro function by its self-cleavage activity. To study P1 protease regulation, we used bioinformatic analysis and in vitro activity experiments to map the core C-terminal catalytic domain. We present evidence that the hypervariable region that precedes the protease domain is predicted as intrinsically disordered, and that it behaves as a negative regulator of P1 proteolytic activity in in vitro cleavage assays. In viral infections, removal of the P1 protease antagonistic regulator is associated with greater symptom severity, induction of salicylate-dependent pathogenesis-related proteins, and reduced viral loads. We suggest that fine modulation of a viral protease activity has evolved to keep viral amplification below host-detrimental levels, and thus to maintain higher long-term replicative capacity.

2020-08-11 | PXD017769 | Pride

Sucrose metabolism in haloarchaea: reassessment using genomics, proteomics and metagenomics

Project description:We used quantitative proteomics (8-plex iTRAQ labeling) to investigate pathways and enzymes potentially important for sucrose metabolism in the halophilic archaeon Halohasta litchfieldiae. The data provided insights into the dynamics of the Hht. litchfieldiae proteome in response to sucrose, advancing the understanding of sucrose and fructose metabolism in haloarchaea.

2019-01-31 | PXD010137 | Pride

Quantitative proteomics of biofilm formation of the Antarctic archaeon Halorubrum lacusprofundi

Project description:Halorubrum lacusprofundi is an important member of Deep Lake in Antarctica, representing ~10% of the lake population (DeMaere et al., 2013). Deep Lake is in the Vestfold Hills, East Antarctica (68°33’36.8S, 78°11’48.7E) and is 36 m deep, monomictic, and perennially cold (down to -20°C) (DeMaere et al., 2013; Williams et al., 2014; Tschitschko et al., 2015; Tschitschko et al., 2016). In this project, using quantitative proteomics (8-plex iTRAQ labeling), proteins, pathways and cellular processes important for biofilm formation were determined for Hrr. lacusprofundi. The data provided a new level of understanding about molecular mechanisms and regulatory networks involved in adaptation of Hrr. lacusprofundi to biofilm formation. DeMaere, M. Z., Williams, T. J., Allen, M. A., Brown, M. V., Gibson, J. A., Rich, J., et al. (2013) High level of intergenera gene exchange shapes the evolution of haloarchaea in an isolated Antarctic lake. Proc Natl Acad Sci USA 110: 16939-16944. Tschitschko, B., Williams, T. J., Allen, M. A., Páez-Espino, D., Kyrpides, N., Zhong, L., et al. (2015) Antarctic archaea–virus interactions: metaproteome-led analysis of invasion, evasion and adaptation. ISME J 9: 2094-2107. Tschitschko, B., Williams, T. J., Allen, M. A., Zhong, L., Raftery, M. J., and Cavicchioli, R. (2016) Ecophysiological distinctions of haloarchaea from a hypersaline Antarctic lake determined using metaproteomics. Appl Environ Microbiol 82: 3165 – 3173. Williams, T. J., Allen, M. A., DeMaere, M. Z., Kyrpides, N. C., Tringe, S. G., Woyke, T., and Cavicchioli, R. (2014) Microbial ecology of an Antarctic hypersaline lake: genomic assessment of ecophysiology among dominant haloarchaea. ISME J 8: 1645-1658.

2016-12-13 | PXD004202 | Pride

Quantitative proteomics of cold adaptation of the Antarctic archaeon Halohasta litchfieldiae and Halorubrum lacusprofundi

Project description:Halohasta litchfieldiae and Halorubrum lacusprofundi are important members of Deep Lake in Antarctica, representing ~44% (the most abundance) and ~10% (the 3rd most abundance) of the lake population. Deep Lake is in the Vestfold Hills, East Antarctica (68°33’36.8S, 78°11’48.7E) and is 36 m deep, monomictic, and perennially cold (down to -20C) (DeMaere et al., 2013; Williams et al., 2014; Tschitschko et al., 2015; Tschitschko et al., 2016). In this project, using quantitative proteomics (8-plex iTRAQ labeling), proteins, pathways and cellular processes important for cold adaptation were determined for both Hht. litchfieldiae and Hrr. lacusprofundi. The data provided a new level of understanding about molecular mechanisms and regulatory networks involved in adaptation of the Antarctic haloarchaea to cold environment. DeMaere, M. Z., Williams, T. J., Allen, M. A., Brown, M. V., Gibson, J. A., Rich, J., et al. (2013) High level of intergenera gene exchange shapes the evolution of haloarchaea in an isolated Antarctic lake. Proc Natl Acad Sci USA 110: 16939-16944. Tschitschko, B., Williams, T. J., Allen, M. A., Páez-Espino, D., Kyrpides, N., Zhong, L., et al. (2015) Antarctic archaea–virus interactions: metaproteome-led analysis of invasion, evasion and adaptation. ISME J 9: 2094-2107. Tschitschko, B., Williams, T. J., Allen, M. A., Zhong, L., Raftery, M. J., and Cavicchioli, R. (2016) Ecophysiological distinctions of haloarchaea from a hypersaline Antarctic lake determined using metaproteomics. Appl Environ Microbiol 82: 3165 – 3173. Williams, T. J., Allen, M. A., DeMaere, M. Z., Kyrpides, N. C., Tringe, S. G., Woyke, T., and Cavicchioli, R. (2014) Microbial ecology of an Antarctic hypersaline lake: genomic assessment of ecophysiology among dominant haloarchaea. ISME J 8: 1645-1658.

2017-02-27 | PXD005076 | Pride

ESCRTIII-associated protein AtALIX mediates high affinity phosphate transporter trafficking to maintain phosphate homeostasis in Arabidopsis

Project description:Prior to the release of their cargoes into the vacuolar lumen, sorting endosomes mature into multivesicular bodies (MVB) through the action of ENDOSOMAL COMPLEX REQUIRED FOR TRANSPORT (ESCRT) protein complexes. MVB-mediated sorting of high affinity phosphate transporters (PHT1) to the vacuole limits their plasma membrane levels under phosphate sufficient conditions, a process that allows plants to maintain phosphate homeostasis. We describe here AtALIX, a cytosolic protein that associates to MVB by interacting with ESCRT-III subunit SNF7 and enables PHT1;1 trafficking to the vacuole. Thus, we show that the partial loss of function mutant Atalix-1 displays reduced vacuolar degradation of PHT1;1. AtALIX versions containing the Atalix-1 mutation showed reduced interaction with SNF7, providing a simple molecular explanation for impaired cargo trafficking in Atalix-1 mutants. Indeed, Atalix-1 mutation also hampered vacuolar sorting of brassinosteroid receptor BRI1. In line with a presumed broad target spectrum, Atalix-1 mutation is pleiotropic, provoking reduced plant growth, late flowering and altered vacuole morphogenesis, whereas null mutants are lethal, indicating that AtALIX controls diverse processes in plants being essential for their life.

2015-09-09 | PXD002075 | Pride

Effect of purification of galactooligosaccharides derived from lactulose with Saccharomyces cerevisiae on their capacity to bind immune cell receptor Dectin-2

Project description:Lactulose-derived oligosaccharides (OsLu) are prebiotic galactooligosaccharides (GOS) known to be beneficial for human health. Many of these carbohydrates are reported to have immunomodulatory properties; however the molecular mechanism is unclear. OsLu produced by enzymatic synthesis can be purified with Saccharomyces cerevisiae (OsLu-Sc). We show that this purification method introduces yeast-derived proteins reactive to Dectin-2, an innate immune receptor for fungal polysaccharides. Using a cell-based bioassay, we tested the binding of OsLu and GOS samples to Dectin-2. While OsLu purified with active charcoal and commercial GOS failed to bind to Dectin-2, we found OsLu-Sc bound to this receptor. The carbohydrate-binding incompetent mutant of Dectin-2 failed to bind to OsLu-Sc. These data suggest that OsLu-Sc introduced carbohydrate ligands for Dectin-2. In accordance with this, proteomic analysis revealed OsLu-Sc contained S. cerevisiae-derived mannoproteins. Therefore, our data highlights the importance of the purification method for OsLu, which may positively affect the bioactivity of OsLu.

2018-12-11 | PXD010495 | Pride

Response of the Biomining Acidithiobacillus ferrooxidans to high Cadmium Concentrations

Project description:Cadmium is one of several heavy metals present in contaminated soils. Apparently, it has no biological role but can produce DNA damage, overexpression of stress response proteins and misfolded proteins, amongst other deleterial effects. Acidithiobacillus ferrooxidans is an acidophilic bacterium capable of resisting very high concentrations of heavy metals such as cadmium. This is important for industrial bioleaching processes where Cd+2 concentrations can be in the range of 5-100 mM. Cadmium resistance mechanisms in these microorganisms have not been fully characterized. A. ferrooxidans ATCC 53993 contains genes coding for possible metal resistance determinants such as efflux systems belonging to three families: P-type ATPases, RND transporters and cation diffusion facilitators (CDF). In addition, it has some extra copies of these genes in its exclusive genomic island (GI). Several of these putative genes were characterized in the present report by determining their transcriptional expression profiles and functionality. Moreover, a global quantitative proteomic analysis was carried out to further explore new cadmium resistance determinants in this biomining acidophile. Changes in iron oxidation pathways, upregulation of transport proteins (P-type ATPases and CDFs) and changes in ribosomal protein levels were seen. Finally, increased concentrations of exclusive putative cadmium ATPases present in strain ATCC 53993 GI and other non-identified proteins such as Lferr_0210, which forms part of a possible operon, could explain its greater resistance to cadmium compared to other acidophiles such as A. ferrooxidans ATCC 23270.

2022-02-28 | PXD012041 | Pride

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