Discovery of bacterial polyhydroxyalkanoate synthase (PhaC)-encoding genes from seasonal Baltic Sea ice and cold estuarine waters

Extremophiles

Volumn 19, Issue 1, 2015, Pages 197-206

  Pärnänen, Katariina ^a   Karkman, Antti ^a   Virta, Marko ^a   Eronen Rasimus, Eeva ^b,c   Kaartokallio, Hermanni ^b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b FINNISH ENVIRONMENT INSTITUTE   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Bioplastics; Cold adaptation; Polyhydroxyalkanoate synthase genes (phaC); Polyhydroxyalkanoates (PHA); Sea ice

Indexed keywords

ACYLTRANSFERASE; CARBON; MACROMOLECULE; POLY(3-HYDROXYALKANOIC ACID) SYNTHASE; SEA WATER;

BACTERIUM; CHEMISTRY; COLD; DNA SEQUENCE; ECOSYSTEM; ENZYMOLOGY; GENETICS; GEOGRAPHY; ICE COVER; MACROMOLECULE; MICROBIOLOGY; PHYLOGENY; SEASON;

ACYLTRANSFERASES; BACTERIA; CARBON; COLD TEMPERATURE; ECOSYSTEM; GEOGRAPHY; ICE COVER; MACROMOLECULAR SUBSTANCES; PHYLOGENY; SEASONS; SEAWATER; SEQUENCE ANALYSIS, DNA;

EID: 84921936870     PISSN: 14310651     EISSN: 14334909     Source Type: Journal    
DOI: 10.1007/s00792-014-0699-9     Document Type: Article

References (59)

1. Alfreider A, Vogt C, Babel W (2002) Microbial diversity in an in situ reactor system treating monochlorobenzene contaminated groundwater as revealed by 16S ribosomal DNA analysis. Syst Appl Microbiol 25:232–240
2. Alvarez HM, Pucci OH, Steinbüchel A (1997) Lipid storage compounds in marine bacteria. Appl Microbiol Biotechnol 47:132–139
3. Amon RMW, Fitznar HP, Benner R (2001) Linkages among the bioreactivity, chemical composition, and diagenetic state of marine dissolved organic matter. Limnol Oceanogr 46:287–297
4. Anderson AJ, Dawes EA (1990) Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoates. Microbiol Rev 54:450–472
5. Arahal DR, Lekunberri I, Gonzalez JM, Pascual J, Pujalte MJ, Pedros-Alio C, Pinhassi J (2007) Neptuniibacter caesariensis gen. nov., sp nov., a novel marine genome-sequenced gammaproteobacterium. Int J Syst Evol Microbiol 57:1000–1006
6. Asmala E, Autio R, Kaartokallio H, Pitkanen L, Stedmon CA, Thomas DN (2013) Bioavailability of riverine dissolved organic matter in three Baltic Sea estuaries and the effect of catchment land use. Biogeosciences 10:6969–6986
7. Ayub ND, Tribelli PM, Lopez NI (2009) Polyhydroxyalkanoates are essential for maintenance of redox state in the Antarctic bacterium Pseudomonas sp 14-3 during low temperature adaptation. Extremophiles 13:59–66
8. Berlanga M, Montero MT, Fernandez-Borrell J, Guerrero R (2006) Rapid spectrofluorometric screening of poly-hydroxyalkanoate-producing bacteria from microbial mats. Int Microbiol 9:95–102
9. Calace N, Castrovinci D, Maresca V, Petronio BM, Pietroletti M, Scardala S (2001) Aquatic humic substances in pack ice-seawater-sediment system. Int J Environ Anal Chem 79:315–329
10. Cho JC, Giovannoni SJ (2004) Robiginitalea biformatagen. nov., sp nov., a novel marine bacterium in the family Flavobacteriaceae with a higher G+C content. Int J Syst Evol Microbiol 54:1101–1106
11. Connon S, Tovanabootr A, Dolan M, Vergin K, Giovannoni S, Semprini L (2005) Bacterial community composition determined by culture-independent and -dependent methods during propane-stimulated bioremediation in trichloroethene-contaminated groundwater. Environ Microbiol 7:165–178
12. Cota GF, Prinsenberg SJ, Bennett EB, Loder JW, Lewis MR, Anning JL, Watson NHF, Harris LR (1987) Nutrient fluxes during extended blooms of Arctic ice algae. J Geophys Res Oceans 92:1951–1962
13. Criscuolo A, Gribaldo S (2010) BMGE (block mapping and gathering with entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol 10:210
14. Deming JW (2010) Sea ice bacteria and viruses. In: Thomas DN, Dieckmann GS (eds) Sea ice, 2nd edn. Wiley-Blackwell, Oxford, pp 247–282
15. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
16. Feller G, Gerday C (2003) Psychrophilic enzymes: Hot topics in cold adaptation. Nat Rev Microbiol 1:200–208
17. Finneran KT, Johnsen CV, Lovley DR (2003) Rhodoferax ferrireducens sp nov., a psychrotolerant, facultatively anaerobic bacterium that oxidizes acetate with the reduction of Fe(III). Int J Syst Evol Microbiol 53:669–673
18. Godoy F, Vancanneyt M, Martinez M, Steinbuchel A, Swings J, Rehm BHA (2003) Sphingopyxis chilensis sp nov., a chlorophenol-degrading bacterium that accumulates polyhydroxyalkanoate, and transfer of Sphingomonas alaskensis to Sphingopyxis alaskensis comb. nov. Int J Syst Evol Microbiol 53:473–477
19. Granskog M, Kaartokallio H, Kuosa H, Thomas DN, Vainio J (2006) Sea ice in the Baltic Sea—a review. Estuar Coast Shelf Sci 70:145–160
20. Hobbie JE, Daley RJ, Jasper S (1977) Use of nuclepore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33:1225–1228
21. Ishige T, Tani A, Sakai Y, Kato N (2003) Wax ester production by bacteria. Curr Op Microbiol 6:244–250
22. Kaartokallio H (2004) Food web components, and physical and chemical properties of Baltic Sea ice. Mar Ecol Prog Ser 273:49–63
23. Kaartokallio H, Kuosa H, Thomas DN, Granskog MA, Kivi K (2007) Biomass, composition and activity of organism assemblages along a salinity gradient in sea ice subjected to river discharge in the Baltic Sea. Polar Biol 30:183–197
24. Kaartokallio H, Sogaard DH, Norman L, Rysgaard S, Tison J-, Delille B, Thomas DN (2013) Short-term variability in bacterial abundance, cell properties, and incorporation of leucine and thymidine in subarctic sea ice. Aquat Microb Ecol 71:57–73
25. Kadouri D, Jurkevitch E, Okon Y, Castro-Sowinski S (2005) Ecological and agricultural significance of bacterial polyhydroxyalkanoates. Crit Rev Microbiol 31:55–67
26. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780
27. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066
28. Koller M, Gasser I, Schmid F, Berg G (2011) Linking ecology with economy: insights into polyhydroxyalkanoate-producing microorganisms. Eng Life Sci 11:222–237
29. Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291
30. Krell A, Funck D, Plettner I, John U, Dieckmann G (2007) Regulation of proline metabolism under salt stress in the psychrophilic diatom Fragilariopsis cylindrus (Bacillariophyceae). J Phycol 43:753–762
31. Krembs C, Deming JW (2008) The role of exopolymers in microbial adaptation to sea ice. In: Margesin R, Schinner F, Marx J et al (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Heidelberg, pp 247–264
32. Krembs C, Eicken H, Deming JW (2011) Exopolymer alteration of physical properties of sea ice and implications for ice habitability and biogeochemistry in a warmer Arctic. Proc Natl Acad Sci USA 108:3653–3658
33. Lee SY (1996) Bacterial polyhydroxyalkanoates. Biotechnol Bioeng 49:1–14
34. Lopez NI, Julia Pettinari M, Stackebrandt E, Tribelli PM, Potter M, Steinbuechel A, Mendez BS (2009) Pseudomonas extremaustralis sp. nov., a poly(3-hydroxybutyrate) producer isolated from an Antarctic environment. Curr Microbiol 59:514–519
35. Madigan MT, Jung DO, Woese CR, Achenbach LA (2000) Rhodoferax antarcticus sp. nov., a moderately psychrophilic purple nonsulfur bacterium isolated from an Antarctic microbial mat. Arch Microbiol 173:269–277
36. Madison LL, Huisman GW (1999) Metabolic engineering of poly(3-hydroxyalkanoates): from DNA to plastic. Microbiol Mol Biol R 63:21–53
37. Margesin R, Feller G (2010) Biotechnological applications of psychrophiles. Environ Technol 31:835–844
38. Mattes TE, Alexander AK, Richardson PM, Munk AC, Han CS, Stothard P, Coleman NV (2008) The genome of Polaromonas sp strain JS666: Insights into the evolution of a hydrocarbon- and xenobiotic-degrading bacterium, and features of relevance to biotechnology. Appl Environ Microbiol 74:6405–6416
39. Methe BA, Nelson KE, Deming JW, Momen B, Melamud E, Zhang XJ, Moult J, Madupu R, Nelson WC, Dodson RJ, Brinkac LM, Daugherty SC, Durkin AS, DeBoy RT, Kolonay JF, Sullivan SA, Zhou LW, Davidsen TM, Wu M, Huston AL, Lewis M, Weaver B, Weidman JF, Khouri H, Utterback TR, Feldblyum TV, Fraser CM (2005) The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc Natl Acad Sci USA 102:10913–10918
40. Ostle AG, Holt JG (1982) Nile blue A as a fluorescent stain for poly-beta-hydroxybutyrate. Appl Environ Microbiol 44:238–241
41. Pomeroy LR, Wiebe WJ (2001) Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat Microb Ecol 23:187–204
42. Rehm BHA (2003) Polyester synthases: natural catalysts for plastics. Biochem J 376:15–33
43. Rehm BHA (2010) Bacterial polymers: biosynthesis, modifications and applications. Nat Rev Microbiol 8:578–592
44. Reusch RN, Sadoff HL (1988) Putative structure and functions of a poly-beta-hydroxybutyrate calcium polyphosphate channel in bacterial plasma membranes. Proc Natl Acad Sci USA 85:4176–4180
45. Risso C, Sun J, Zhuang K, Mahadevan R, DeBoy R, Ismail W, Shrivastava S, Huot H, Kothari S, Daugherty S, Bui O, Schilling CH, Lovley DR, Methe BA (2009) Genome-scale comparison and constraint-based metabolic reconstruction of the facultative anaerobic Fe(III)-reducer Rhodoferax ferrireducens. BMC Genom 10:447
46. Staden R (1996) The Staden sequence analysis package. Mol Biotechnol 5:233–241
47. Stamatakis A, Ott M, Ludwig T (2005) RAxML-OMP: An efficient program for phylogenetic inference on SMPs. In: 8th International Conference on Parallel Computing Technologies 3606, pp 288–302
48. Stedmon CA, Thomas DN, Papadimitriou S, Granskog MA, Dieckmann GS (2011) Using fluorescence to characterize dissolved organic matter in Antarctic sea ice brines. J Geophys Res Biogeo 116:G03027
49. Tal S, Okon Y (1985) Production of the reserve material poly-beta-hydroxybutyrate and its function in Azospirillum brasilense Cd. Can J Microbiol 31:608–613
50. Thomas DN, Lara RJ, Eicken H, Kattner G, Skoog A (1995) Dissolved organic matter in Arctic multiyear sea ice during winter—major components and relationship to ice characteristics. Polar Biol 15:477–483
51. Ting L, Williams TJ, Cowley MJ, Lauro FM, Guilhaus M, Raftery MJ, Cavicchioli R (2010) Cold adaptation in the marine bacterium, Sphingopyxis alaskensis, assessed using quantitative proteomics. Environ Microbiol 12:2658–2676
52. Tribelli PM, Lopez NI (2011) Poly(3-hydroxybutyrate) influences biofilm formation and motility in the novel Antarctic species Pseudomonas extremaustralis under cold conditions. Extremophiles 15:541–547
53. Tribelli PM, Raiger Iustman LJ, Catone MV, Di Martino C, Revale S, Mendez BS, Lopez NI (2012) Genome sequence of the polyhydroxybutyrate producer Pseudomonas extremaustralis, a highly stress-resistant Antarctic bacterium. J Bacteriol 194:2381–2382
54. Underwood GJC, Fietz S, Papadimitriou S, Thomas DN, Dieckmann GS (2010) Distribution and composition of dissolved extracellular polymeric substances (EPS) in Antarctic sea ice. Mar Ecol Prog Ser 404:1–19
55. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115
56. Vezzi A, Campanaro S, D’Angelo M, Simonato F, Vitulo N, Lauro FM, Cestaro A, Malacrida G, Simionati B, Cannata N, Romualdi C, Bartlett DH, Valle G (2005) Life at depth: Photobacterium profundum genome sequence and expression analysis. Science 307:1459–1461
57. Villanueva L, Navarrete A, Urmeneta J, Geyer R, White DC, Guerrero R (2007) Monitoring diel variations of physiological status and bacterial diversity in an estuarine microbial mat: an integrated biomarker analysis. Microb Ecol 54:523–531
58. Wältermann M, Steinbüchel A (2005) Neutral lipid bodies in prokaryotes: recent insights into structure, formation, and relationship to eukaryotic lipid deposits. J Bacteriol 187:3607–3619
59. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinform 13:134