Abstract
At elevated osmolarity of the mineral medium M63, marine macroalgae constitute important osmoprotectants and nutrients sources for Escherichia coli. Growth of bacterial population (16 strains) was improved by supplementing M63 salts medium with either aqueous or ethanolic algal extracts obtained from Ascophyllum nodosum, Fucus serratus, Enteromorpha ramulosa, Ulva lactuca, and Palmaria palmata. In their presence, growth was still observed even at 1.02 m NaCl. Furthermore, the E. coli ZB400 growth in presence of whole macroalgae thalli in M63/0.85 m NaCI reached its maximum within 24 h (5 × 107 − 5 × 108 colony-forming units [CFU] per milliliter). In the presence of A. nodosum, bacterial growth was inhibited. In the same experimental conditions, ethanolic extracts improved E. coli growth significantly, because the yield reached 1011 CFU per milliliter. Ulva lactuca and P. palmata allowed the better growth. The Dragendorff-positive compounds extracted from bacterial cells growing on each ethanolic extract exhibited an osmoprotective effect as proved by a disk-diffusion assay. On the other hand, the -onium compounds (quaternary ammonium [betaines] and tertiary sulphonium) and total free amino acid contents of U. lactuca ethanolic extracts were higher than in others. Fucaceae extracts demonstrated especially high protein content. Algal extracts constitute not only an appreciable osmoprotection source for E. coli but also nutrient sources.
Similar content being viewed by others
References
Anderson IC, Rhodes M, Kator H (1979) Sublethal stress in Escherichia coli: a function of salinity. Appl Environ Microbiol 38:1147–1152
Anthoni U, Christophersen C, Hougaard L, Nielsen PH (1991) Quarternary ammonium compounds in the biosphere—An example of a versatile adaptive strategy. Comp Biochem Physiol 99B:1–18
Blunden G, Gordon SM (1986) Betaines and their sulphonio analogues in marine algae. In: Round FE, Chapman DJ (eds) Progress in phycological research, vol. 4. Biopress, Bristol, England, pp 39–80
Blunden G, Smith BE, Irons MW, Yang M-H, Roch OG, Patel AV (1992) Betaines and their sulphonium compounds from 62 species of marine algae. Biochem System Ecol 20:373–388
Britten RJ, McClure FT (1962) The amino acid pool in E. coli. Bacteriol Rev 26:292–335
Carlucci AF, Pramer D (1960) An evaluation of factors affecting the survival of Escherichia coli in sea water. II. Salinity, pH, and nutrients. Appl Microbiol 8:247–250
Chai TJ (1983) Characteristics of Escherichia coli grown in bay water as compared with rich medium. Appl Environ Microbiol 45:1316–1323
Chambers ST, Kunin CM, Miller D, Hamada A (1987) Dimethylthetin can substitute for glycine betaine as an osmoprotectant molecule for Escherichia coli. J Bacteriol 169:4845–4847
Christian JHB (1955) The water relations of growth and respiration of Salmonella oranienburg at 30°C. Aust J Biol Sci 8:490–497
Cohen GN, Rickenberg HV (1956) Concentration spécifique reversible des amino acides chez Escherichia coli. Ann Inst Pasteur (Paris) 91:693–720
Colwell RR, Brayton PR, Grimes DJ, Roszak DB, Hug SA, Palmer LM (1985) Viable but nonculturable Vibrio cholerae and related pathogens in the environment: implications for release of genetically engineered microorganisms. Bio/Technology 3:817–820
Csonka LN (1981) Proline over-production results in enhanced osmotolerance in Salmonella typhimurium. Mol Gen Genet 182:82–86
Csonka LN, Hanson AD (1991) Prokaryotic osmoregulation: genetics and physiology. Annu Rev Microbiol 45:569–606
Dickson DM, Wyn Jones RG, Davenport J (1980) Steady state osmotic adaptation in Ulva lactuca. Planta 150:158–165
Edwards DM, Reed RH, Chudek JA, Foster R, Stewart WDP (1987) Organic solute accumulation in osmotically-stressed Enteromorpha intestinalis. Mar Biol 95:583–592
Edwards DM, Reed RH, Stewart WDP (1988) Osmoacclimatation in Enteromorpha intestinalis: long-term effects of osmotic stress on organic solute accumulation. Mar Biol 98:467–476
Flatau GN, Clement RL, Gauthier MJ, Puel DC (1992) Effect of incubation of Escherichia coli cells with halophyte extracts on their subsequent survival in seawater. Can J Microbiol 38:838–842
Gauthier MJ, Le Rudulier D (1990) Survival in seawater of Escherichia coli cells grown in marine sediments containing glycin betaïn. Appl Environ Microbiol 56:2915–2918
Gerba CP, McLeod JS (1976) Effect of sediments on the survival of Escherichia coli in marine waters. Appl Environ Microbiol 32:114–120
Ghoul M, Bernard T, Cormier M (1990) Evidence that Escherichia coli accumulates glycine betaine from marine sediments. Appl Environ Microbiol 56:551–554
Grimes DJ, Atwell RW, Brayton PR, Palmer LM, Rollins DM, Roszak DB, Singleton FL, Tamplin ML, Colwell RR (1986) The fate of enteric pathogenic bacteria in estuarine and marine environments. Microbiol Sci 3:324–329
Grimes DJ, Colwell RR (1986) Viability and virulence of Escherichia coli suspended by membrane chamber in semi-tropical ocean water. FEMS Microbiol Lett 34:161–165
Hanes NB, Fragala R (1967) Effect of sea water concentration on survival of indicator bacteria. J Water Pollution Control Federation 39:97–104
Larsen PI, Sydnes LK, Landfald B, Strøm AR (1987) Osmoregulation in Escherichia coli by accumulation of organic osmolytes: betaines, glutamic acid, and trehalose. Arch Microbiol 147:1–7
Le Rudulier D, Bouillard L (1983) Glycine betaine, an osmotic effector in Klebsiella pneumoniae and other members of the Enterobacteriaceae. Appl Environ Microbiol 46:152–159
Le Rudulier D, Stróm AR, Dandekar AM, Smith LT, Valentine RC (1984) Molecular biology of osmoregulation. Science 224:1064–1068
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Lustigman B, Brown C (1991) Antibiotic production by marine algae isolated from the New York/New Jersey coast. Bull Environ Contam Toxicol 46:329–335
Lustigman B, Lee HL, Thees N, Masucci J (1992) Production of antibacterial substances by macroalgae of the New York/New Jersey coast, USA. Bull Environ Contam Toxicol 49:743–749
Matsumoto J, Omura T (1980) Some factors affecting the survival of fecal indicator bacteria in sea water. Technol Rep Tohoku Univ 45:169–185
Measures JC (1975) Role of amino acids in osmoregulation of non halophilic bacteria. Nature (London) 257:398–400
Perroud B, Le Rudulier D (1985) Glycine betaine transport in Escherichia coli: osmotic modulation. J Bacteriol 161:393–401
Reed RH (1983) The osmotic response of Polysiphonia lanosa (L.) Tandy from marine and estuarine sites: evidence for incomplete recovery of turgor. J Exp Mar Biol Ecol 68:169–193
Rhodes MW, Kator H (1988) Survival of Escherichia coli and Salmonella spp. in estuarine environments. Appl Environ Microbiol 54:2902–2907
Storey R, Wyn Jones RG (1977) Quaternary ammonium compounds in plants in relation to salt resistance. Phytochemistry 16:447–453
Tempest DW Meers JL, Brown CM (1970) Influence of environment on the content and composition of microbial free amino acid pools. J Gen Microbiol 64:171–185
Wall IS, Christianson DD, Dimler RJ, Senti FR (1960) Spectrophotometric determination of betaines and other quaternary nitrogen compounds as their periodides. Anal Chem 32:870–874
Wyn Jones RG, Storey R (1981) Betaines. In: Physiology and biochemistry of drought resistance. In: Paleg LC, Aspinall D (eds) Plants. Academic Press, New York, pp 171–235
Xu HS, Roberts N, Singleton FL, Atwell RW Grimes DJ, Colwell RR (1982) Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb Ecol 8:313–323
Yemm EW, Cocking EC (1955) The determination of amino-acids with ninhydrin. Analyst 80:209–213
Author information
Authors and Affiliations
Additional information
Correspondence to: J. Minet
Rights and permissions
About this article
Cite this article
Ghoul, M., Minet, J., Bernard, T. et al. Marine macroalgae as a source for osmoprotection for Escherichia coli . Microb Ecol 30, 171–181 (1995). https://doi.org/10.1007/BF00172572
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00172572