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Comparison of the compatible solute pool of two slightly halophilic planctomycetes species, Gimesia maris and Rubinisphaera brasiliensis

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Abstract

Gimesia maris and Rubinisphaera brasiliensis are slightly halophilic representatives of the deep-branching phylum Planctomycetes. For osmoadaptation both species accumulated α-glutamate, sucrose, ectoine and hydroxyectoine. A major role was found for ectoine, hydroxyectoine as well as sucrose under hyper-osmotic shock conditions. Nevertheless, the levels of sucrose were up-regulated by the increased salinity levels and also by low nitrogen availability. Additionally, G. maris accumulated glucosylglycerate (GG) as major solute specifically under low nitrogen levels, which prompted us to analyse the transcript abundance of two homologues genes known for the biosynthesis of GG, namely glucosyl-3-phosphoglycerate synthase (GpgS) and glucosyl-3-phosphoglycerate phosphatase (GpgP). By qPCR using a suitable reference gene selected in this study, the transcript abundance of the biosynthetic genes was quantified in G. maris cells under hyper-osmotic shock or under low nitrogen conditions. The gpgS gene was induced under nitrogen-limiting conditions suggesting that GG synthesis is regulated primarily at the transcription level. Moreover, the expression of a gene coding for a putative sucrose-phosphorylase (Spase) located upstream the gpgS and gpgP genes was up-regulated, predicting a metabolic role of Spase probably related to GG synthesis.

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References

  • Alarico S, Costa M, Sousa MS et al (2014) Mycobacterium hassiacum recovers from nitrogen starvation with up-regulation of a novel glucosylglycerate hydrolase and depletion of the accumulated glucosylglycerate. Sci Rep 4:6766

    Article  PubMed  Google Scholar 

  • Andersen CL, Jensen JL, Orntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR Data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64:5245–5250

    Article  CAS  PubMed  Google Scholar 

  • Barrett T, Troup DB, Wilhite SE et al (2007) NCBI GEO: mining tens of millions of expression profiles database and tools update. Nucleic Acids Res 35:D760–D765

    Article  CAS  PubMed  Google Scholar 

  • Behrends V, Williams KJ, Jenkins VA, Robertson BD, Bundy JG (2012) Free glucosylglycerate is a novel marker of nitrogen stress in Mycobacterium smegmatis. J Proteome Res 11:3888–3896

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Brown AD (1976) Microbial water stress. Bacteriol Rev 40:803–846

    CAS  PubMed  PubMed Central  Google Scholar 

  • Buckley DH, Huangyutitham V, Nelson T, Rumberger A, Thies JE (2006) Diversity of Planctomycetes in soil in relation to soil history and environmental heterogeneity. Appl Env Microbiol 72:4522–4531

    Article  CAS  Google Scholar 

  • Cánovas D, Borges N, Vargas C, Ventosa A, Nieto JJ, Santos H (1999) Role of Nγ-Acetyldiaminobutyrate as an enzyme stabilizer and an intermediate in the biosynthesis of hydroxyectoine. Appl Environ Microbiol 65:3774–3779

    PubMed  PubMed Central  Google Scholar 

  • Cayrou C, Raoult D, Drancourt M (2010) Broad-spectrum antibiotic resistance of Planctomycetes organisms determined by Etest. J Antimicrob Chemother 65:2119–2122

    Article  CAS  PubMed  Google Scholar 

  • Costa J, Empadinhas N, da Costa MS (2007) Glucosylglycerate biosynthesis in the deepest lineage of the Bacteria: characterization of the thermophilic proteins GpgS and GpgP from Persephonella marina. J Bacteriol 189:1648–1654

    Article  CAS  PubMed  Google Scholar 

  • Cunha S, D’Avó AF, Mingote A, Lamosa P, da Costa MS, Costa J (2013) Mannosylglucosylglycerate biosynthesis in the deep-branching phylum Planctomycetes: characterization of the uncommon enzymes from Rhodopirellula baltica. Sci Rep 3

  • D’Avó AF, Cunha S, Mingote A, Lamosa P, da Costa MS, Costa J (2013) A unique pool of compatible solutes on Rhodopirellula baltica, member of the deep-branching phylum Planctomycetes. PLoS One 8:e68289

    Article  PubMed  PubMed Central  Google Scholar 

  • da Costa MS, Santos H, Galinski EA (1998) An overview of the role and diversity of compatible solutes in Bacteria and Archaea. Adv Biochem Eng Biotechnol 61:117–153

    PubMed  Google Scholar 

  • Empadinhas N, da Costa MS (2010) Diversity, biological roles and biosynthetic pathways for sugar-glycerate containing compatible solutes in bacteria and archaea. Environ Microbiol 13:2056–2077

    Article  PubMed  Google Scholar 

  • Fernandes C, Empadinhas N, da Costa MS (2007) Single-step pathway for synthesis of glucosylglycerate in Persephonella marina. J Bacteriol 189:4014–4019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuerst J, Sagulenko E (2011) Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nat Rev Microbiol 9:403–413

    Article  CAS  PubMed  Google Scholar 

  • Goude R, Renaud S, Bonnassie S, Bernard T, Blanco C (2004) Glutamine, glutamate, and α-glucosylglycerate are the major osmotic solutes accumulated by Erwinia chrysanthemi strain 3937. Appl Environ Microbiol 70:6535–6541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hagemann M, Marin K (1999) Salt-induced sucrose accumulation is mediated by sucrose-phosphate-synthase in Cyanobacteria. J Plant Physiol 155:424–430

    Article  CAS  Google Scholar 

  • Jeske O, Jogler M, Petersen J, Sikorski J, Jogler C (2013) From genome mining to phenotypic microarrays: planctomycetes as source for novel bioactive molecules. Antonie Van Leeuwenhoek 104:551–567

    Article  CAS  PubMed  Google Scholar 

  • Khmelenina VN, Kalyuzhnaya MG, Sakharovsky VG, Snzina NE, Trotsenko YA, Gottschalk G (1999) Osmoadaptation in halophilic and alkaliphilic methanotrophs. Arch Microbiol 172:321–329

    Article  CAS  PubMed  Google Scholar 

  • Klähn S, Hagemann M (2011) Compatible solute biosynthesis in cyanobacteria: cyanobacterial solutes. Environ Microbiol 13:551–562

    Article  PubMed  Google Scholar 

  • Klähn S, Steglich C, Hess WR, Hagemann M (2010) Glucosylglycerate: a secondary compatible solute common to marine cyanobacteria from nitrogen-poor environments. Environ Microbiol 12:83–94

    Article  PubMed  Google Scholar 

  • Lage OM, Bondoso J (2014) Planctomycetes and macroalgae, a striking association. Front Microbiol 5:267

    Article  PubMed  PubMed Central  Google Scholar 

  • Lamosa P, Rodrigues MV, Gonçalves LG et al (2013) Organic solutes in the deepest phylogenetic branches of the Bacteria: identification of α(1–6)glucosyl-α(1–2)glucosylglycerate in Persephonella marina. Extremophiles 17:137–146

    Article  CAS  PubMed  Google Scholar 

  • Lunn JE (2002) Evolution of sucrose synthesis. Plant Physiol 128:1490–1500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris RM, Longnecker K, Giovannoni SJ (2006) Pirellula and OM43 are among the dominant lineages identified in an Oregon coast diatom bloom. Environ Microbiol 8:1361–1370

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30(9):e36

    Article  PubMed  PubMed Central  Google Scholar 

  • Roberts MF (2005) Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Systems 1:5

    Article  PubMed  PubMed Central  Google Scholar 

  • Robertson DE, Lai M-C, Gunsalus RP, Roberts MF (1992) Composition, variation, and dynamics of major osmotic solutes in Methanohalophilus Strain FDF1. Appl Environ Microbiol 58:2438–2443

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sawangwan T, Goedl C, Nidetzky B (2009) Single-step enzymatic synthesis of (R)-2-O-α-d-glucopyranosyl glycerate, a compatible solute from microorganisms that functions as a protein stabiliser. Org Biomol Chem 7:4267–4270

    Article  CAS  PubMed  Google Scholar 

  • Scheuner C, Tindall BJ, Lu M et al (2014) Complete genome sequence of Planctomyces brasiliensis type strain (DSM 5305T), phylogenomic analysis and reclassification of Planctomycetes including the descriptions of Gimesia gen. nov., Planctopirus gen. nov. and Rubinisphaera gen. nov. and emended descriptions of the order Planctomycetales and the family Planctomycetaceae. Stand Genomic Sci. 9:10

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:7

    Article  Google Scholar 

  • Wecker P, Klockow C, Ellrott A, Quast C, Langhammer P, Harder J, Glöckner F (2009) Transcriptional response of the model planctomycete Rhodopirellula baltica SH1T to changing environmental conditions. BMC Genom 10:410

    Article  Google Scholar 

  • Wegner C-E, Richter-Heitmann T, Klindworth A et al (2013) Expression of sulfatases in Rhodopirellula baltica and the diversity of sulfatases in the genus Rhodopirellula. Mar Genomics 9:51–61

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by FEDER funds through the Operational Programme Competitiveness Factors—COMPETE and the strategic project UID/NEU/04539/2013. Catarina Ferreira acknowledge scholarship from FCT (SFRH/BD/68366/2010). The NMR spectrometers are part of the National NMR Facility supported by Fundação para a Ciência e a Tecnologia (RECI/BBB-BQB/0230/2012). We are especially grateful to Helena Santos and her group (ITQB, Oeiras, Portugal) for valuable collaboration.

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Authors and Affiliations

  1. Center for Neuroscience and Cell Biology, University of Coimbra, 3004-504, Coimbra, Portugal

    Catarina Ferreira & Milton S. da Costa

  2. Department of Medical Sciences and Institute for Biomedicine-iBiMED, University of Aveiro, 3810-193, Aveiro, Portugal

    Ana R. Soares & Manuel A. Santos

  3. Centro de Ressonância Magnética António Xavier, Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, 2781-901, Oeiras, Portugal

    Pedro Lamosa

Authors
  1. Catarina Ferreira
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  2. Ana R. Soares
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  3. Pedro Lamosa
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  4. Manuel A. Santos
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  5. Milton S. da Costa
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Corresponding author

Correspondence to Milton S. da Costa.

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Communicated by A. Oren.

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Ferreira, C., Soares, A.R., Lamosa, P. et al. Comparison of the compatible solute pool of two slightly halophilic planctomycetes species, Gimesia maris and Rubinisphaera brasiliensis . Extremophiles 20, 811–820 (2016). https://doi.org/10.1007/s00792-016-0868-0

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  • DOI: https://doi.org/10.1007/s00792-016-0868-0

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