Skip to main content

Adaptations of Cold- and Pressure-Loving Bacteria to the Deep-Sea Environment: Cell Envelope and Flagella

  • Chapter
  • First Online:
Microbial Ecology of Extreme Environments

Abstract

Compared to terrestrial environments our knowledge of microorganisms inhabiting oceans, the largest ecosystem on Earth, is limited. Deep oceans contain bacteria that thrive at high pressure and low temperature. For them, as for all bacteria, the outer structures of the cell are the first point of contact with the environment, both sensing and being modified in response to it. The vast majority of studied cold- and pressure-loving bacteria are Gram-negative and so in this chapter, the adaptations of their cell envelope and flagella are presented. In deep-sea bacteria, the structure of phospholipids and lipopolysaccharides is modified in order to maintain membrane fluidity and enable membrane-localised proteins to perform their functions. Many of the membrane proteins involved in nutrient acquisition, transport, respiration, sensing and signalling are also specifically adapted to function at high pressure and low temperature. The ability to move towards nutrients or away from hostile environment is extremely important for bacterial survival and yet very vulnerable to increased pressure. Deep-sea bacteria are capable of swimming even at 150 MPa, which suggests their motility systems are specifically adapted to high pressure. Moreover, some bacteria have been shown to produce a second type of flagella (lateral flagella) in response to high pressure or low temperature. The findings presented in this chapter are a result of many techniques and analyses applied to whole microbial communities, single species as well as particular genes and proteins. Investigation of the adaptations to high pressure and low temperature not only expands basic knowledge but also identifies targets that could have biotechnological and industrial application. Deep-sea bacteria could be used for production of biofuels, secondary metabolites of value for drug development, and various pressure and temperature adapted enzymes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abe F (2007) Exploration of the effects of high hydrostatic pressure on microbial growth, physiology and survival: perspectives from piezophysiology. Biosci Biotechnol Biochem 71:2347–2357

    Article  CAS  PubMed  Google Scholar 

  • Abe F (2013) Dynamic structural changes in microbial membranes in response to high hydrostatic pressure analyzed using time-resolved fluorescence anisotropy measurement. Biophys Chem 183:3–8

    Article  CAS  PubMed  Google Scholar 

  • Abe F, Horikoshi K (2000) Tryptophan permease gene TAT2 confers high-pressure growth in Saccharomyces cerevisiae. Mol Cell Biol 20:8093–8102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abe F, Horikoshi K (2001) The biotechnological potential of piezophiles. Trends Biotechnol 19:102–108

    Article  CAS  PubMed  Google Scholar 

  • Abu-Lail NI, Camesano TA (2003) Role of lipopolysaccharides in the adhesion, retention, and transport of Escherichia coli JM109. Environ Sci Technol 37:2173–2183

    Article  CAS  PubMed  Google Scholar 

  • Aertsen A, Meersman F, Hendrickx ME, Vogel RF, Michiels CW (2009) Biotechnology under high pressure: applications and implications. Trends Biotechnol 27:434–441

    Article  CAS  PubMed  Google Scholar 

  • Allcock D (2009) Investigating the molecular basis of cold temperature and high pressure adapted growth in Photobacterium profundum SS9. Ph.D. thesis, University of Edinburgh, Edinburgh, Scotland, UK

    Google Scholar 

  • Allen EE, Bartlett DH (2000) FabF is required for piezoregulation of cis-vaccenic acid levels and piezophilic growth of the deep-sea bacterium Photobacterium profundum strain SS9. J Bacteriol 182:1264–1271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allen EE, Facciotti D, Bartlett DH (1999) Monounsaturated but not polyunsaturated fatty acids are required for growth of the deep-sea bacterium Photobacterium profundum SS9 at high pressure and low temperature. Appl Environ Microbiol 65:1710–1720

    CAS  PubMed  PubMed Central  Google Scholar 

  • Almagro-Moreno S, Root MZ, Taylor RK (2015a) Role of ToxS in the proteolytic cascade of virulence regulator ToxR in Vibrio cholerae. Mol Microbiol 98:963–976

    Google Scholar 

  • Almagro-Moreno S, Kim TK, Skorupski K, Taylor RK (2015b) Proteolysis of virulence regulator ToxR is associated with entry of Vibrio cholerae into a dormant state. PLoS Genet 11:e1005145

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Amiri-Jami M, Griffiths MW (2010) Recombinant production of omega-3 fatty acids in Escherichia coli using a gene cluster isolated from Shewanella baltica MAC1. J Appl Microbiol 109:1897–1905

    Article  CAS  PubMed  Google Scholar 

  • Baker MA, Inoue Y, Takeda K, Ishijima A, Berry RM (2011) Two methods of temperature control for single-molecule measurements. Eur Biophys J 40:651–660

    Article  CAS  PubMed  Google Scholar 

  • Bartlett DH (1991) Pressure sensing in deep-sea bacteria. Res Microbiol 142:923–925

    Article  CAS  PubMed  Google Scholar 

  • Bartlett DH (1999) Microbial adaptations to the psychrosphere/piezosphere. J Mol Microbiol Biotechnol 1:93–100

    CAS  PubMed  Google Scholar 

  • Bartlett DH (2002) Pressure effects on in vivo microbial processes. Biochim Biophys Acta 1595:367–381

    Article  CAS  PubMed  Google Scholar 

  • Bartlett D, Chi E (1994) Genetic characterization of ompH mutants in the deep-sea bacterium Photobacterium sp. strain SS9. Arch Microbiol 162:323–328

    Article  CAS  PubMed  Google Scholar 

  • Bartlett DH, Welch TJ (1995) ompH gene expression is regulated by multiple environmental cues in addition to high pressure in the deep-sea bacterium Photobacterium species strain SS9. J Bacteriol 177:1008–1016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bartlett D, Wright M, Yayanos AA, Silverman M (1989) Isolation of a gene regulated by hydrostatic pressure in a deep-sea bacterium. Nature 342:572–574

    Article  CAS  PubMed  Google Scholar 

  • Bartlett DH, Ferguson GP, Valle G (2008) Adaptations of the psychrotolerant piezophile Photobacterium profundum strain SS9. In: Michiels C, Bartlett DH, Aertsen A (eds) High-pressure microbiology. American Society for Microbiology Press, Washington, DC, pp 319–337

    Google Scholar 

  • Beck BJ, Connolly LE, De Las Penas A, Downs DM (1997) Evidence that rseC, a gene in the rpoE cluster, has a role in thiamine synthesis in Salmonella typhimurium. J Bacteriol 179:6504–6508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belas R (2014) Biofilms, flagella, and mechanosensing of surfaces by bacteria. Trends Microbiol 22:517–527

    Article  CAS  PubMed  Google Scholar 

  • Beveridge TJ (1999) Structures of Gram-negative cell walls and their derived membrane vesicles. J Bacteriol 181:4725–4733

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bidle KA, Bartlett DH (2001) RNA arbitrarily primed PCR survey of genes regulated by ToxR in the deep-sea bacterium Photobacterium profundum strain SS9. J Bacteriol 183:1688–1693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bina J, Zhu J, Dziejman M, Faruque S, Calderwood S, Mekalanos J (2003) ToxR regulon of Vibrio cholerae and its expression in vibrios shed by cholera patients. Proc Natl Acad Sci USA 100:2801–2806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowman JP, Gosink JJ, McCammon SA, Lewis TE, Nichols DS, Nichols PD, Skerratt JH, Staley JT, McMeekin TA (1998) Colwellia demingiae sp. nov., Colwellia hornerae sp. nov., Colwellia rossensis sp. nov. and Colwellia psychrotropica sp. nov.: psychrophilic Antarctic species with the ability to synthesize docosahexaenoic acid (22:6ω3). Int J Syst Bacteriol 48:1171–1180

    Article  CAS  Google Scholar 

  • Buschmann S, Warkentin E, Xie H, Langer JD, Ermler U, Michel H (2010) The structure of cbb 3 cytochrome oxidase provides insights into proton pumping. Science 329:327–330

    Article  CAS  PubMed  Google Scholar 

  • Campanaro S, Vezzi A, Vitulo N, Lauro FM, D’Angelo M, Simonato F, Cestaro A, Malacrida G, Bertoloni G et al (2005) Laterally transferred elements and high pressure adaptation in Photobacterium profundum strains. BMC Genomics 6:122

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Campanaro S, Treu L, Valle G (2008) Protein evolution in deep sea bacteria: an analysis of amino acids substitution rates. BMC Evol Biol 8:313

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Campanaro S, Pascale FD, Telatin A, Schiavon R, Bartlett DH, Valle G (2012) The transcriptional landscape of the deep-sea bacterium Photobacterium profundum in both a toxR mutant and its parental strain. BMC Genomics 13:567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carlson RW, Sanders RE, Napoli C, Albersheim P (1978) Host-symbiont interactions: III. Purification and partial characterization of Rhizobium lipopolysaccharides. Plant Physiol 62:912–917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chi E, Bartlett DH (1993) Use of a reporter gene to follow high-pressure signal transduction in the deep-sea bacterium Photobacterium sp. strain SS9. J Bacteriol 175:7533–7540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chi E, Bartlett DH (1995) An rpoE-like locus controls outer membrane protein synthesis and growth at cold temperatures and high pressures in the deep-sea bacterium Photobacterium sp. strain SS9. Mol Microbiol 17:713–726

    Article  CAS  PubMed  Google Scholar 

  • Chikuma S, Kasahara R, Kato C, Tamegai H (2007) Bacterial adaptation to high pressure: a respiratory system in the deep-sea bacterium Shewanella violacea DSS12. FEMS Microbiol Lett 267:108–112

    Article  CAS  PubMed  Google Scholar 

  • Corsaro MM, Lanzetta R, Parrilli E, Parrilli M, Tutino ML, Ummarino S (2004) Influence of growth temperature on lipid and phosphate contents of surface polysaccharides from the antarctic bacterium Pseudoalteromonas haloplanktis TAC 125. J Bacteriol 186:29–34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deckers-Hebestreit G, Altendorf K (1996) The F0F1-type ATP synthases of bacteria: structure and function of the F0 complex. Annu Rev Microbiol 50:791–824

    Article  CAS  PubMed  Google Scholar 

  • DeLong EF (1986) Adaptations of deep-sea bacteria to the abyssal environment. Ph.D. thesis, University of California, San Diego, USA

    Google Scholar 

  • DeLong EF, Franks DG, Yayanos AA (1997) Evolutionary relationships of cultivated psychrophilic and barophilic deep-sea bacteria. Appl Environ Microbiol 63:2105–2108

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deming JW (1998) Deep ocean environmental biotechnology. Curr Opin Biotechnol 9:283–287

    Article  CAS  PubMed  Google Scholar 

  • DiRita VJ, Mekalanos JJ (1991) Periplasmic interaction between two membrane regulatory proteins, ToxR and ToxS, results in signal transduction and transcriptional activation. Cell 64:29–37

    Article  CAS  PubMed  Google Scholar 

  • Duarte C (2006) Introduction. In: Duarte C (ed) The exploration of marine biodiversity: scientific and technological challenges. Fundación BBVA, Bilbao, p 7

    Google Scholar 

  • Dziejman M, Mekalanos JJ (1994) Analysis of membrane protein interaction: ToxR can dimerize the amino terminus of phage lambda repressor. Mol Microbiol 13:485–494

    Article  CAS  PubMed  Google Scholar 

  • El-Hajj ZW, Tryfona T, Allcock DJ, Hasan F, Lauro FM, Sawyer L, Bartlett DH, Ferguson GP (2009) Importance of proteins controlling initiation of DNA replication in the growth of the high-pressure-loving bacterium Photobacterium profundum SS9. J Bacteriol 191:6383–6393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Hajj ZW, Allcock D, Tryfona T, Lauro FM, Sawyer L, Bartlett DH, Ferguson GP (2010) Insights into piezophily from genetic studies on the deep-sea bacterium, Photobacterium profundum SS9. Ann NY Acad Sci 1189:143–148

    Article  CAS  PubMed  Google Scholar 

  • Eloe EA, Lauro FM, Vogel RF, Bartlett DH (2008) The deep-sea bacterium Photobacterium profundum SS9 utilizes separate flagellar systems for swimming and swarming under high-pressure conditions. Appl Environ Microbiol 74:6298–6305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erhardt M, Namba K, Hughes KT (2010) Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harb Perspect Biol 2:a000299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1:200–208

    Article  CAS  PubMed  Google Scholar 

  • Gardel CL, Mekalanos JJ (1994) Regulation of cholera toxin by temperature, pH, and osmolarity. Methods Enzymol 235:517–526

    Article  CAS  PubMed  Google Scholar 

  • Gattis SG, Chung HS, Trent MS, Raetz CR (2013) The origin of 8-amino-3,8-dideoxy-D-manno-octulosonic acid (Kdo8N) in the lipopolysaccharide of Shewanella oneidensis. J Biol Chem 288:9216–9225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gode-Potratz CJ, Kustusch RJ, Breheny PJ, Weiss DS, McCarter LL (2011) Surface sensing in Vibrio parahaemolyticus triggers a programme of gene expression that promotes colonization and virulence. Mol Microbiol 79:240–263

    Article  CAS  PubMed  Google Scholar 

  • Hayden JD, Ades SE (2008) The extracytoplasmic stress factor, σE, is required to maintain cell envelope integrity in Escherichia coli. PLoS ONE 3:e1573

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hazel JR, Williams EE (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167–227

    Article  CAS  PubMed  Google Scholar 

  • Jannasch HW, Taylor CD (1984) Deep-sea microbiology. Annu Rev Microbiol 38:487–514

    Article  CAS  PubMed  Google Scholar 

  • Jian H, Xiao X, Wang F (2013) Role of filamentous phage SW1 in regulating the lateral flagella of Shewanella piezotolerans strain WP3 at low temperatures. Appl Environ Microbiol 79:7101–7109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jian H, Xiong L, He Y, Xiao X (2015) The regulatory function of LexA is temperature-dependent in the deep-sea bacterium Shewanella piezotolerans WP3. Front Microbiol 6:627

    Article  PubMed  PubMed Central  Google Scholar 

  • Junge K, Eicken H, Deming JW (2004) Bacterial activity at −2 to 20 °C in Arctic wintertime sea ice. Appl Environ Microbiol 70:550–557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kato C, Bartlett DH (1997) The molecular biology of barophilic bacteria. Extremophiles 1:111–116

    Article  CAS  PubMed  Google Scholar 

  • Kato C, Qureshi MH (1999) Pressure response in deep-sea piezophilic bacteria. J Mol Microbiol Biotechnol 1:87–92

    CAS  PubMed  Google Scholar 

  • Kato C, Li L, Nogi Y, Nakamura Y, Tamaoka J, Horikoshi K (1998) Extremely barophilic bacteria isolated from the Mariana Trench, Challenger Deep, at a depth of 11,000 meters. Appl Environ Microbiol 64:1510–1513

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kato M, Hayashi R, Tsuda T, Taniguchi K (2002) High pressure-induced changes of biological membrane. Study on the membrane-bound Na+/K+-ATPase as a model system. Eur J Biochem 269:110–118

    Article  CAS  PubMed  Google Scholar 

  • Kautharapu KB, Rathmacher J, Jarboe LR (2013) Growth condition optimization for docosahexaenoic acid (DHA) production by Moritella marina MP-1. Appl Microbiol Biotechnol 97:2859–2866

    Article  CAS  PubMed  Google Scholar 

  • Kawamoto J, Kurihara T, Yamamoto K, Nagayasu M, Tani Y, Mihara H, Hosokawa M, Baba T, Sato SB et al (2009) Eicosapentaenoic acid plays a beneficial role in membrane organization and cell division of a cold-adapted bacterium, Shewanella livingstonensis Ac10. J Bacteriol 191:632–640

    Article  CAS  PubMed  Google Scholar 

  • Kawamoto J, Sato T, Nakasone K, Kato C, Mihara H, Esaki N, Kurihara T (2011) Favourable effects of eicosapentaenoic acid on the late step of the cell division in a piezophilic bacterium, Shewanella violacea DSS12, at high-hydrostatic pressures. Environ Microbiol 13:2293–2298

    Article  CAS  PubMed  Google Scholar 

  • Kearns DB (2010) A field guide to bacterial swarming motility. Nat Rev Microbiol 8:634–644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kierek K, Watnick PI (2003) The Vibrio cholerae O139 O-antigen polysaccharide is essential for Ca2 +-dependent biofilm development in sea water. Proc Natl Acad Sci USA 100:14357–14362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knirel YA, Lindner B, Vinogradov E, Shaikhutdinova RZ, Senchenkova SN, Kocharova NA, Holst O, Pier GB, Anisimov AP (2005) Cold temperature-induced modifications to the composition and structure of the lipopolysaccharide of Yersinia pestis. Carbohydr Res 340:1625–1630

    Article  CAS  PubMed  Google Scholar 

  • Korenevsky A, Beveridge TJ (2007) The surface physicochemistry and adhesiveness of Shewanella are affected by their surface polysaccharides. Microbiology 153:1872–1883

    Article  CAS  PubMed  Google Scholar 

  • Korenevsky AA, Vinogradov E, Gorby Y, Beveridge TJ (2002) Characterization of the lipopolysaccharides and capsules of Shewanella spp. Appl Environ Microbiol 68:4653–4657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar GS, Jagannadham MV, Ray MK (2002) Low-temperature-induced changes in composition and fluidity of lipopolysaccharides in the Antarctic psychrotrophic bacterium Pseudomonas syringae. J Bacteriol 184:6746–6749

    Article  CAS  PubMed  Google Scholar 

  • Lauro FM, Eloe EA, Liverani N, Bertoloni G, Bartlett DH (2005) Conjugal vectors for cloning, expression, and insertional mutagenesis in Gram-negative bacteria. Biotechniques 38:708–712

    Article  CAS  PubMed  Google Scholar 

  • Lauro FM, Chastain RA, Blankenship LE, Yayanos AA, Bartlett DH (2007) The unique 16S rRNA genes of piezophiles reflect both phylogeny and adaptation. Appl Environ Microbiol 73:838–845

    Article  CAS  PubMed  Google Scholar 

  • Lauro FM, Tran K, Vezzi A, Vitulo N, Valle G, Bartlett DH (2008) Large-scale transposon mutagenesis of Photobacterium profundum SS9 reveals new genetic loci important for growth at low temperature and high pressure. J Bacteriol 190:1699–1709

    Article  CAS  PubMed  Google Scholar 

  • Le Bihan T, Rayner J, Roy MM, Spagnolo L (2013) Photobacterium profundum under pressure: a MS-based label-free quantitative proteomics study. PLoS ONE 8:e60897

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McCarter L, Hilmen M, Silverman M (1988) Flagellar dynamometer controls swarmer cell differentiation of V. parahaemolyticus. Cell 54:345–351

    Article  CAS  PubMed  Google Scholar 

  • McElhaney RN (1982) Effects of membrane lipids on transport and enzymatic activities. In: Razin S, Rottem S (eds) Current topics in membranes and transport. Academic Press, New York, pp 317–380

    Google Scholar 

  • Meganathan R, Marquis RE (1973) Loss of bacterial motility under pressure. Nature 246:525–527

    Article  CAS  PubMed  Google Scholar 

  • Merino S, Shaw JG, Tomas JM (2006) Bacterial lateral flagella: an inducible flagella system. FEMS Microbiol Lett 263:127–135

    Article  CAS  PubMed  Google Scholar 

  • Miller VL, Mekalanos JJ (1988) A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170:2575–2583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Missiakas D, Raina S (1998) The extracytoplasmic function sigma factors: role and regulation. Mol Microbiol 28:1059–1066

    Article  CAS  PubMed  Google Scholar 

  • Muskotal A, Kiraly R, Sebestyen A, Gugolya Z, Vegh BM, Vonderviszt F (2006) Interaction of FliS flagellar chaperone with flagellin. FEBS Lett 580:3916–3920

    Article  CAS  PubMed  Google Scholar 

  • Myka KK (2013) Investigating the genetic requirements for high pressure- and cold-adapted growth in Photobacterium profundum SS9. Ph.D. thesis, University of Aberdeen, Aberdeen, Scotland, UK

    Google Scholar 

  • Nazarenko EL, Komandrova NA, Gorshkova RP, Tomshich SV, Zubkov VA, Kilcoyne M, Savage AV (2003) Structures of polysaccharides and oligosaccharides of some Gram-negative marine Proteobacteria. Carbohydr Res 338:2449–2457

    Article  CAS  PubMed  Google Scholar 

  • Nazarenko EL, Crawford RJ, Ivanova EP (2011) The structural diversity of carbohydrate antigens of selected Gram-negative marine bacteria. Mar Drugs 9:1914–1954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nogi Y, Masui N, Kato C (1998a) Photobacterium profundum sp. nov., a new, moderately barophilic bacterial species isolated from a deep-sea sediment. Extremophiles 2:1–7

    Article  CAS  PubMed  Google Scholar 

  • Nogi Y, Kato C, Horikoshi K (1998b) Moritella japonica sp. nov., a novel barophilic bacterium isolated from a Japan Trench sediment. J Gen Appl Microbiol 44:289–295

    Article  CAS  PubMed  Google Scholar 

  • Ohke Y, Sakoda A, Kato C, Sambongi Y, Kawamoto J, Kurihara T, Tamegai H (2013) Regulation of cytochrome c- and quinol oxidases, and piezotolerance of their activities in the deep-sea piezophile Shewanella violacea DSS12 in response to growth conditions. Biosci Biotechnol Biochem 77:1522–1528

    Article  CAS  PubMed  Google Scholar 

  • Okuyama H, Orikasa Y, Nishida T (2008) Significance of antioxidative functions of eicosapentaenoic and docosahexaenoic acids in marine microorganisms. Appl Environ Microbiol 74:570–574

    Article  CAS  PubMed  Google Scholar 

  • Orikasa Y, Nishida T, Hase A, Watanabe K, Morita N, Okuyama H (2006) A phosphopantetheinyl transferase gene essential for biosynthesis of n-3 polyunsaturated fatty acids from Moritella marina strain MP-1. FEBS Lett 580:4423–4429

    Article  CAS  PubMed  Google Scholar 

  • Ottemann KM, Mekalanos JJ (1995) Analysis of Vibrio cholerae ToxR function by construction of novel fusion proteins. Mol Microbiol 15:719–731

    Article  CAS  PubMed  Google Scholar 

  • Oyola-Robles D, Rullan-Lind C, Carballeira NM, Baerga-Ortiz A (2014) Expression of dehydratase domains from a polyunsaturated fatty acid synthase increases the production of fatty acids in Escherichia coli. Enzyme Microb Technol 55:133–139

    Article  CAS  PubMed  Google Scholar 

  • Post DM, Yu L, Krasity BC, Choudhury B, Mandel MJ, Brennan CA, Ruby EG, McFall-Ngai MJ, Gibson BW et al (2012) O-antigen and core carbohydrate of Vibrio fischeri lipopolysaccharide: composition and analysis of their role in Euprymna scolopes light organ colonization. J Biol Chem 287:8515–8530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qureshi MH, Kato C, Horikoshi K (1998a) Purification of a ccb-type quinol oxidase specifically induced in a deep-sea barophilic bacterium, Shewanella sp. strain DB-172F. Extremophiles 2:93–99

    Article  CAS  PubMed  Google Scholar 

  • Qureshi MH, Kato C, Horikoshi K (1998b) Purification of two pressure-regulated c-type cytochromes from a deep-sea barophilic bacterium, Shewanella sp. strain DB-172F. FEMS Microbiol Lett 161:301–309

    Article  CAS  Google Scholar 

  • Raetz CR, Whitfield C (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71:635–700

    Article  CAS  PubMed  Google Scholar 

  • Ray MK, Kumar GS, Shivaji S (1994) Phosphorylation of lipopolysaccharides in the Antarctic psychrotroph Pseudomonas syringae: a possible role in temperature adaptation. J Bacteriol 176:4243–4249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodrigues DF, Tiedje JM (2008) Coping with our cold planet. Appl Environ Microbiol 74:1677–1686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rottem S, Leive L (1977) Effect of variations in lipopolysaccharide on the fluidity of the outer membrane of Escherichia coli. J Biol Chem 252:2077–2081

    CAS  PubMed  Google Scholar 

  • Schild S, Lamprecht AK, Reidl J (2005) Molecular and functional characterization of O-antigen transfer in Vibrio cholerae. J Biol Chem 280:25936–25947

    Article  CAS  PubMed  Google Scholar 

  • Schuhmacher JS, Thormann KM, Bange G (2015) How bacteria maintain location and number of flagella? FEMS Microbiol Rev 39:812–822

    Article  PubMed  Google Scholar 

  • Sheng H, Lim JY, Watkins MK, Minnich SA, Hovde CJ (2008) Characterization of an Escherichia coli O157:H7 O-antigen deletion mutant and effect of the deletion on bacterial persistence in the mouse intestine and colonization at the bovine terminal rectal mucosa. Appl Environ Microbiol 74:5015–5022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shivaji S, Prakash JS (2010) How do bacteria sense and respond to low temperature? Arch Microbiol 192:85–95

    Article  CAS  PubMed  Google Scholar 

  • Silhavy TJ, Kahne D, Walker S (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2:a000414

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Simonato F, Campanaro S, Lauro FM, Vezzi A, D’Angelo M, Vitulo N, Valle G, Bartlett DH (2006) Piezophilic adaptation: a genomic point of view. J Biotechnol 126:11–25

    Article  CAS  PubMed  Google Scholar 

  • Sinensky M (1974) Homeoviscous adaptation—a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc Natl Acad Sci USA 71:522–525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solov’eva T, Davydova V, Krasikova I, Yermak I (2013) Marine compounds with therapeutic potential in Gram-negative sepsis. Mar Drugs 11:2216–2229

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Soutourina OA, Bertin PN (2003) Regulation cascade of flagellar expression in Gram-negative bacteria. FEMS Microbiol Rev 27:505–523

    Article  CAS  PubMed  Google Scholar 

  • Stach JE, Bull AT (2005) Estimating and comparing the diversity of marine actinobacteria. Antonie Van Leeuwenhoek 87:3–9

    Article  PubMed  Google Scholar 

  • Strauss J, Burnham NA, Camesano TA (2009) Atomic force microscopy study of the role of LPS O-antigen on adhesion of E. coli. J Mol Recognit 22:347–355

    Article  CAS  PubMed  Google Scholar 

  • Sweet CR, Watson RE, Landis CA, Smith JP (2015) Temperature-dependence of lipid A acyl structure in Psychrobacter cryohalolentis and Arctic isolates of Colwellia hornerae and Colwellia piezophila. Mar Drugs 13:4701–4720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamegai H, Kawano H, Ishii A, Chikuma S, Nakasone K, Kato C (2005) Pressure-regulated biosynthesis of cytochrome bd in piezo- and psychrophilic deep-sea bacterium Shewanella violacea DSS12. Extremophiles 9:247–253

    Article  CAS  PubMed  Google Scholar 

  • Tamegai H, Nishikawa S, Haga M, Bartlett DH (2012) The respiratory system of the piezophile Photobacterium profundum SS9 grown under various pressures. Biosci Biotechnol Biochem 76:1506–1510

    Article  CAS  PubMed  Google Scholar 

  • Toguchi A, Siano M, Burkart M, Harshey RM (2000) Genetics of swarming motility in Salmonella enterica serovar Typhimurium: critical role for lipopolysaccharide. J Bacteriol 182:6308–6321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trujillo U, Vazquez-Rosa E, Oyola-Robles D, Stagg LJ, Vassallo DA, Vega IE, Arold ST, Baerga-Ortiz A (2013) Solution structure of the tandem acyl carrier protein domains from a polyunsaturated fatty acid synthase reveals beads-on-a-string configuration. PLoS ONE 8:e57859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai CM, Frasch CE (1982) A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119:115–119

    Article  CAS  PubMed  Google Scholar 

  • Usui K, Hiraki T, Kawamoto J, Kurihara T, Nogi Y, Kato C, Abe F (2012) Eicosapentaenoic acid plays a role in stabilizing dynamic membrane structure in the deep-sea piezophile Shewanella violacea: a study employing high-pressure time-resolved fluorescence anisotropy measurement. Biochim Biophys Acta 1818:574–583

    Article  CAS  PubMed  Google Scholar 

  • Vezzi A, Campanaro S, D’Angelo M, Simonato F, Vitulo N, Lauro FM, Cestaro A, Malacrida G, Simionati B et al (2005) Life at depth: Photobacterium profundum genome sequence and expression analysis. Science 307:1459–1461

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Wang J, Jian H, Zhang B, Li S, Zeng X, Gao L, Bartlett DH, Yu J et al (2008) Environmental adaptation: genomic analysis of the piezotolerant and psychrotolerant deep-sea iron reducing bacterium Shewanella piezotolerans WP3. PLoS ONE 3:e1937

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang F, Xiao X, Ou HY, Gai Y, Wang F (2009) Role and regulation of fatty acid biosynthesis in the response of Shewanella piezotolerans WP3 to different temperatures and pressures. J Bacteriol 191:2574–2584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welch TJ, Bartlett DH (1996) Isolation and characterization of the structural gene for OmpL, a pressure-regulated porin-like protein from the deep-sea bacterium Photobacterium species strain SS9. J Bacteriol 178:5027–5031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welch TJ, Bartlett DH (1998) Identification of a regulatory protein required for pressure-responsive gene expression in the deep-sea bacterium Photobacterium species strain SS9. Mol Microbiol 27:977–985

    Article  CAS  PubMed  Google Scholar 

  • Welch TJ, Farewell A, Neidhardt FC, Bartlett DH (1993) Stress response of Escherichia coli to elevated hydrostatic pressure. J Bacteriol 175:7170–7177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitfield C, Amor PA, Koplin R (1997) Modulation of the surface architecture of Gram-negative bacteria by the action of surface polymer: lipid A-core ligase and by determinants of polymer chain length. Mol Microbiol 23:629–638

    Article  CAS  PubMed  Google Scholar 

  • Williams PG (2009) Panning for chemical gold: marine bacteria as a source of new therapeutics. Trends Biotechnol 27:45–52

    Article  CAS  PubMed  Google Scholar 

  • Winter R, Dzwolak W (2005) Exploring the temperature-pressure configurational landscape of biomolecules: from lipid membranes to proteins. Philos Trans A Math Phys Eng Sci 363:537–562 (discussion 562-533)

    Google Scholar 

  • Wollenweber HW, Schlecht S, Luderitz O, Rietschel ET (1983) Fatty acid in lipopolysaccharides of Salmonella species grown at low temperature. Identification and position. Eur J Biochem 130:167–171

    Article  CAS  PubMed  Google Scholar 

  • Wollmann P, Zeth K (2007) The structure of RseB: a sensor in periplasmic stress response of E. coli. J Mol Biol 372:927–941

    Article  CAS  PubMed  Google Scholar 

  • Wu L, Wang J, Tang P, Chen H, Gao H (2011) Genetic and molecular characterization of flagellar assembly in Shewanella oneidensis. PLoS ONE 6:e21479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie L, Altindal T, Chattopadhyay S, Wu XL (2011) Bacterial flagellum as a propeller and as a rudder for efficient chemotaxis. Proc Natl Acad Sci USA 108:2246–2251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada M, Nakasone K, Tamegai H, Kato C, Usami R, Horikoshi K (2000) Pressure regulation of soluble cytochromes c in a deep-sea piezophilic bacterium, Shewanella violacea. J Bacteriol 182:2945–2952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan J, Berg HC (2010) Thermal and solvent-isotope effects on the flagellar rotary motor near zero load. Biophys J 98:2121–2126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Li X, Bartlett DH, Xiao X (2015) Current developments in marine microbiology: high-pressure biotechnology and the genetic engineering of piezophiles. Curr Opin Biotechnol 33:157–164

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kamila K. Myka .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Myka, K.K. et al. (2017). Adaptations of Cold- and Pressure-Loving Bacteria to the Deep-Sea Environment: Cell Envelope and Flagella. In: Chénard, C., Lauro, F. (eds) Microbial Ecology of Extreme Environments. Springer, Cham. https://doi.org/10.1007/978-3-319-51686-8_3

Download citation

Publish with us

Policies and ethics