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The non-metabolizable sucrose analog sucralose is a potent inhibitor of hormogonium differentiation in the filamentous cyanobacterium Nostoc punctiforme

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Abstract

Nostoc punctiforme is a filamentous cyanobacterium which forms nitrogen-fixing symbioses with several different plants and fungi. Establishment of these symbioses requires the formation of motile hormogonium filaments. Once infected, the plant partner is thought to supply a hormogonium-repressing factor (HRF) to maintain the cyanobacteria in a vegetative, nitrogen-fixing state. Evidence implies that sucrose may serve as a HRF. Here, we tested the effects of sucralose, a non-metabolizable sucrose analog, on hormogonium differentiation. Sucralose inhibited hormogonium differentiation at a concentration approximately one-tenth that of sucrose. This result implies that: (1) sucrose, not a sucrose catabolite, is perceived by the cell and (2) inhibition is not due to a more general osmolarity-dependent effect. Additionally, both sucrose and sucralose induced the accrual of a polysaccharide sheath which bound specifically to the lectin ConA, indicating the presence of α-d-mannose and/or α-d-glucose. A ConA-specific polysaccharide was also found to be expressed in N. punctiforme colonies from tissue sections of the symbiotically grown hornwort Anthoceros punctatus. These findings imply that plant-derived sucrose or sucrose analogs may have multiple effects on N. punctiforme, including both repression of hormogonia and the induction of a polysaccharide sheath that may be essential to establish and maintain the symbiotic state.

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References

  • Bay G, Nahar N, Oubre M, Whitehouse MJ, Wardle DA, Zackrisson O, Nilsson MC, Rasmussen U (2013) Boreal feather mosses secrete chemical signals to gain nitrogen. New Phytol 200:54–60

    Article  CAS  PubMed  Google Scholar 

  • Campbell EL, Meeks JC (1989) Characteristics of hormogonia formation by symbiotic Nostoc spp. in response to the presence of Anthoceros punctatus or its extracellular products. Appl Environ Microbiol 55:125–131

    PubMed Central  CAS  PubMed  Google Scholar 

  • Campbell EL, Wong FC, Meeks JC (2003) DNA binding properties of the HrmR protein of Nostoc punctiforme responsible for transcriptional regulation of genes involved in the differentiation of hormogonia. Mol Microbiol 47:573–582

    Article  CAS  PubMed  Google Scholar 

  • Campbell EL, Summers ML, Christman H, Martin ME, Meeks JC (2007) Global gene expression patterns of Nostoc punctiforme in steady-state dinitrogen-grown heterocyst-containing cultures and at single time points during the differentiation of akinetes and hormogonia. J Bacteriol 189:5247–5256

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Campbell EL, Hagen KD, Chen R, Risser DD, Ferreira DP, Meeks JC (2015) Genetic analysis reveals the identity of the photoreceptor for phototaxis in hormogonium filaments of Nostoc punctiforme. J Bacteriol 197:782–791

    Article  PubMed Central  PubMed  Google Scholar 

  • Cohen MF, Meeks JC (1997) A hormogonium regulating locus, hrmUA, of the cyanobacterium Nostoc punctiforme strain ATCC 29133 and its response to an extract of a symbiotic plant partner Anthoceros punctatus. Mol Plant Microbe Interact 10:280–289

    Article  CAS  PubMed  Google Scholar 

  • Cohen MF, Yamasaki H (2000) Flavonoid-induced expression of a symbiosis-related gene in the cyanobacterium Nostoc punctiforme. J Bacteriol 182:4644–4646

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dedonder R (1966) Levansucrase from Bacillus subtilis. Methods Enzymol 8:500–505

    Article  CAS  Google Scholar 

  • Donovan RS, Robinson CW, Glick BR (1996) Review: Optimizing inducer and culture conditions for expression of foreign proteins under the control of the lac promoter. J Ind Microbiol 16:145–154

    Article  CAS  PubMed  Google Scholar 

  • Downie JA (2010) The roles of extracellular proteins, polysaccharides and signals in the interactions of Rhizobia with legume roots. FEMS Microbiol Rev 34:150–170

    Article  CAS  PubMed  Google Scholar 

  • Edelstein AD, Tsuchida MA, Amodaj N, Pinkard H, Vale RD, Stuurman N (2014) Advanced methods of microscope control using μManager software. J Biol Methods 1:e10

    Article  PubMed Central  PubMed  Google Scholar 

  • Ekman M, Picossi S, Campbell EL, Meeks JC, Flores E (2013) A Nostoc punctiforme sugar transporter necessary to establish a cyanobacterium-plant symbiosis. Plant Physiol 161:1984–1992

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Elbert W, Webber B, Burrows S, Steinkamp J, Budel B, Andreae M, Poschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462

    Article  CAS  Google Scholar 

  • Khamar HJ, Breathwaite EK, Prasse CE, Fraley ER, Secor CR, Chibane FL, Elhai J, Chiu WL (2010) Multiple roles of soluble sugars in the establishment of GunneraNostoc endosymbiosis. Plant Physiol 154:1381–1389

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • López-Igual R, Flores E, Herrero A (2010) Inactivation of a heterocyst-specific invertase indicates a principal role of sucrose catabolism in heterocysts of Anabaena sp. J Bacteriol 192:5526–5533

    Article  PubMed Central  PubMed  Google Scholar 

  • Matros A, Peshev D, Peukert M, Mock H, Van den Ende W (2015) Sugars as hydroxyl radical scavengers: proof-of-concept by studying the fate of sucralose in Arabidopsis. Plant J 82:822–839

    Article  CAS  PubMed  Google Scholar 

  • Meeks JC, Elhai J (2002) Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol Mol Biol Rev 66:94–121

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Navia JL, Walkup RE, Vernon NM, Neiditch DS (1996) Production of sucralose without intermediate isolation of crystalline sucralose-6-ester. US patent 5,498,709 A

  • Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJP, Zuker CS (2001) Mammalian sweet taste receptors. Cell 106:381–390

    Article  CAS  PubMed  Google Scholar 

  • Nilsson M, Rasmussen U, Bergman B (2006) Cyanobacterial chemotaxis to extracts of host and nonhost plants. FEMS Microbiol Ecol 55:382–390

    Article  CAS  PubMed  Google Scholar 

  • Nürnberg DJ, Mariscal V, Bornikoel J, Nieves-Morión M, Krauß N, Herrero A, Maldener I, Flores E, Mullineaux CW (2015) Intercellular diffusion of a fluorescent sucrose analog via the septal junctions in a filamentous cyanobacterium. mBio 6:e02109–e021014

    Article  PubMed Central  PubMed  Google Scholar 

  • Omran A, Ahearn G, Bowers D, Swenson J, Coughlin C (2013) Metabolic effects of sucralose on environmental bacteria. J Toxicol 2013:372986

    PubMed Central  PubMed  Google Scholar 

  • Rai AN, Soderback E, Bergman B (2000) Tansley review no. 116. Cyanobacterium-plant symbioses. New Phytol 147:449–481

    Article  CAS  Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 111:1–61

    Article  Google Scholar 

  • Risser DD, Chew WG, Meeks JC (2014) Genetic characterization of the hmp locus, a chemotaxis-like gene cluster that regulates hormogonium development and motility in Nostoc punctiforme. Mol Microbiol 92:222–233

    Article  CAS  PubMed  Google Scholar 

  • Roberts A, Renwick AG, Sims J, Snodin DJ (2000) Sucralose metabolism and pharmacokinetics in man. Food Chem Toxicol 38(Suppl 2):31–41

    Article  Google Scholar 

  • Rodgers GA, Stewart WDP (1977) The cyanophyte-hepatic symbiosis I. Morphology and physiology. New Phytol 78:441–458

    Article  Google Scholar 

  • Schüßler A, Meyer T, Gehrig H, Kluge M (1997) Variations of lectin binding sites in extracellular glycoconjugates during the life cycle of Nostoc punctiforme, a potentially endosymbiotic cyanobacterium. Eur J Phycol 32:233–239

    Article  Google Scholar 

  • Silvester WB, McNamara PJ (1976) The infection process and ultrastructure of the GunneraNostoc symbiosis. New Phytol 77:135–141

    Article  Google Scholar 

  • Soh L, Connors KA, Brooks BW, Zimmerman J (2011) Fate of sucralose through environmental and water treatment processes and impact on plant indicator species. Environ Sci Technol 45:1363–1369

    Article  CAS  PubMed  Google Scholar 

  • Steinberg NA, Meeks JC (1991) Physiological sources of reductant for nitrogen fixation activity in Nostoc sp. strain UCD 7801 in symbiotic association with Anthoceros punctatus. J Bacteriol 173:7324–7329

    PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Marcos Gridi-Papp for his assistance in sectioning A. punctatus tissue and the Lin-Cereghino laboratory for use of and assistance with their vacuum blotting module.

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Correspondence to Douglas D. Risser.

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Communicated by Erko Stackebrandt.

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Splitt, S.D., Risser, D.D. The non-metabolizable sucrose analog sucralose is a potent inhibitor of hormogonium differentiation in the filamentous cyanobacterium Nostoc punctiforme . Arch Microbiol 198, 137–147 (2016). https://doi.org/10.1007/s00203-015-1171-7

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  • DOI: https://doi.org/10.1007/s00203-015-1171-7

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