Niches of two polysaccharide-degrading Polaribacter isolates from the North Sea during a spring diatom bloom

ISME Journal

Volumn 9, Issue 6, 2015, Pages 1410-1422

  Xing, Peng ^a,b   Hahnke, Richard L ^a,g   Unfried, Frank ^a,c   Markert, Stephanie ^c   Huang, Sixing ^a   Barbeyron, Tristan ^d   Harder, Jens ^a   Becher, Dörte ^e   Schweder, Thomas ^c,e   Glöckner, Frank Oliver ^a,f   Amann, Rudolf I ^a   Teeling, Hanno ^a  

^a MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^b NANJING INSTITUTE OF GEOGRAPHY AND LIMNOLOGY   (China)

^c Institute of Marine Biotechnology eV   (Germany)

^d SORBONNE UNIVERSITÉ   (France)

^e UNIVERSITY OF GREIFSWALD   (Germany)

^f JACOBS UNIVERSITY BREMEN   (Germany)

^g LEIBNIZ INSTITUTE DSMZ GERMAN COLLECTION OF MICROORGANISMS AND CELL CULTURES   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAL BLOOM; BACTERIUM; BIODEGRADATION; DIATOM; GENOMICS; NICHE; PHYTOPLANKTON; POLYSACCHARIDE; PROTEIN; PROTEOMICS;

ATLANTIC OCEAN; NORTH SEA;

ALGAE; BACILLARIOPHYTA; FLAVOBACTERIUM; POLARIBACTER; POLARIBACTER SP. SCB44;

CARBOHYDRATE; CHONDROITIN SULFATE; GLUCAN; LAMINARAN; MANNITOL; POLYSACCHARIDE; PROTEIN; RNA 16S;

BACTERIAL GENOME; CHEMISTRY; DIATOM; ECOSYSTEM; EUTROPHICATION; FLAVOBACTERIACEAE; GENETICS; GENOMICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; NORTH SEA; PHYLOGENY; PHYTOPLANKTON; PLANKTON;

CARBOHYDRATES; CHONDROITIN SULFATES; DIATOMS; ECOSYSTEM; EUTROPHICATION; FLAVOBACTERIACEAE; GENOME, BACTERIAL; GENOMICS; GLUCANS; LIGHT; MANNITOL; NORTH SEA; PHYLOGENY; PHYTOPLANKTON; PLANKTON; POLYSACCHARIDES; PROTEINS; RNA, RIBOSOMAL, 16S;

EID: 84929656246     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2014.225     Document Type: Article

References (75)

1. Akram N, Palovaara J, Forsberg J, Lindh MV, Milton DL, Luo H et al. (2013). Regulation of proteorhodopsin gene expression by nutrient limitation in the marine bacterium Vibrio sp. AND4. Environ Microbiol 15: 1400-1415.
2. Arnosti C. (2008). Functional differences between Arctic seawater and sedimentary microbial communities: contrasts in microbial hydrolysis of complex substrates. FEMS Microb Ecol 66: 343-351.
3. Arnosti C, Steen AD, Ziervogel K, Ghobrial S, Jeffrey WH. (2011). Latitudinal gradients in degradation of marine dissolved organic carbon. PLoS One 6: e28900.
4. Arnosti C, Fuchs BM, Amann R, Passow U. (2012). Contrasting extracellular enzyme activities of particle- associated bacteria from distinct provinces of the North Atlantic Ocean. Front Microbiol 3: 425.
5. Auch AF, von Jan M, Klenk H-P, Göker M. (2010). Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2: 117-134.
6. Barbeyron T, L'Haridon S, Corre E, Kloareg B, Potin P. (2001). Zobellia galactanovorans gen. nov., sp. nov., a marine species of Flavobacteriaceae isolated from a red alga, and classification of [Cytophaga] uliginosa (ZoBell and Upham 1944) Reichenbach 1989 as Zobellia uliginosa gen. nov., comb. nov. Int J Syst Evol Microbiol 51: 985-997.
7. Bauer M, Kube M, Teeling H, Richter M, Lombardot T, Allers E et al. (2006). Whole genome analysis of the marine Bacteroidetes 'Gramella forsetii' reveals adaptations to degradation of polymeric organic matter. Environ Microbiol 8: 2201-2213.
8. Beattie A, Hirst EL, Percival E. (1961). Studies on the metabolism of the Chrysophyceae. Comparative structural investigations on leucosin (chrysolaminarin) separated from diatoms and laminarin from the brown algae. Biochem J 79: 531-537.
9. Bennke CM, Neu TR, Fuchs BM, Amann R. (2013). Mapping glycoconjugate-mediated interactions of marine Bacteroidetes with diatoms. Syst Appl Microbiol 36: 417-425.
10. Bernardet J-F. (2010). Class II. Flavobacteriia class. nov. In: Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ, Ward NL et al. (eds). Bergey's Manual of Systematic Bacteriology. The Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes. Springer: New York, NY, USA, pp 106-314.
11. 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.
12. Calleja ML, Batista F, Peacock M, Kudela R, McCarthy MD. (2013). Changes in compound specific d15N amino acid signatures and d/l ratios in marine dissolved organic matter induced by heterotrophic bacterial reworking. Mar Chem 149: 32-44.
13. DeLorenzo S, Bräuer SL, Edgmont CA, Herfort L, Tebo BM, Zuber P. (2012). Ubiquitous dissolved inorganic carbon assimilation by marine bacteria in the Pacific Northwest coastal ocean as determined by stable isotope probing. PLoS One 7: e46695.
14. Di Camillo CG, Luna GM, Bo M, Giordano G, Corinaldesi C, Bavestrello G. (2012). Biodiversity of prokaryotic communities associated with the ectoderm of Ectopleura crocea (Cnidaria, Hydrozoa). PLoS One 7: e39926.
15. Díez-Vives C, Gasol JM, Acinas SG. (2013). Spatial and temporal variability among marine Bacteroidetes populations in the NW Mediterranean Sea. Syst Appl Microbiol 37: 68-78.
16. Dong S, Yang J, Zhang XY, Shi M, Song XY, Chen XL et al. (2012). Cultivable alginate lyase-excreting bacteria associated with the Arctic brown alga Laminaria. Mar Drugs 10: 2481-2491.
17. Eilers H, Pernthaler J, Peplies J, Glöckner FO, Gerdts G, Amann R. (2001). Isolation of novel pelagic bacteria from the German bight and their seasonal contributions to surface picoplankton. Appl Environ Microbiol 67: 5134-5142.
18. Fernández-Gómez B, Richter M, Schüler M, Pinhassi J, Acinas SG, González JM et al. (2013). Ecology of marine Bacteroidetes: a comparative genomics approach. ISME J 7: 1026-1037.
19. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR et al. (2014). Pfam: the protein families database. Nucleic Acids Res 42: 27.
20. Fukui Y, Abe M, Kobayashi M, Saito H, Oikawa H, Yano Y et al. (2013). Polaribacter porphyrae sp. nov. isolated from the red alga Porphyra yezoensis and emended descriptions of the genus Polaribacter and two Polaribacter species. Int J Syst Evol Microbiol 63: 1665-1672.
21. Gilbert JA, Field D, Swift P, Thomas S, Cummings D, Temperton B et al. (2010). The taxonomic and functional diversity of microbes at a temperate coastal site: a 'multi-omic' study of seasonal and diel temporal variation. PLoS One 5: e15545.
22. Gómez-Consarnau L, González JM, Coll-Lladó M, Gourdon P, Pascher T, Neutze R et al. (2007). Light stimulates growth of proteorhodopsin-containing marine Flavobacteria. Nature 445: 210-213.
23. Gómez-Pereira PR, Fuchs BM, Alonso C, Oliver MJ, van Beusekom JE, Amann R. (2010). Distinct flavobacterial communities in contrasting water masses of the North Atlantic Ocean. ISME J 4: 472-487.
24. Gómez-Pereira PR, Schüler M, Fuchs BM, Bennke C, Teeling H, Waldmann J et al. (2012). Genomic content of uncultured Bacteroidetes from contrasting oceanic provinces in the North Atlantic Ocean. Environ Microbiol 14: 52-66.
25. González JM, Fernández-Gómez B, Fernàndez-Guerra A, Gómez-Consarnau L, Sánchez O, Coll-Lladó M et al. (2008). Genome analysis of the proteorhodopsincontaining marine bacterium Polaribacter sp. MED152 (Flavobacteria). Proc Natl Acad Sci USA 105: 8724-8729.
26. González JM, Pinhassi J, Fernández-Gómez B, Coll-Lladó M, González-Velázquez M, Puigbò P et al. (2011). Genomics of the proteorhodopsin-containing marine flavobacterium Dokdonia sp. Strain MED134. Appl Environ Microbiol 77: 8676-8686.
27. Gosink JJ, Woese CR, Staley JT. (1998). Polaribacter gen. nov., with three new species, P. irgensii sp. nov., P. franzmannii sp. nov. and P. filamentus sp. nov., gas vacuolate polar marine bacteria of the Cytophaga- Flavobacterium-Bacteroides group and reclassification of 'Flectobacillus glomeratus' as Polaribacter glomeratus comb. nov. Int J Syst Bacteriol 48: 223-235.
28. Hahnke RL, Harder J. (2013). Phylogenetic diversity of Flavobacteria isolated from the North Sea on solid media. Syst Appl Microbiol 36: 497-504.
29. Hahnke RL, Bennke CM, Fuchs BM, Mann AJ, Rhiel E, Teeling H et al. (2014). Dilution cultivation of marine heterotrophic bacteria abundant after a spring phytoplankton bloom in the North Sea. Environ Microbiol; doi:10.1111/1462-2920.12479.
30. Heinz E, Williams TA, Nakjang S, Noel CJ, Swan DC, Goldberg AV et al. (2012). The genome of the obligate intracellular parasite Trachipleistophora hominis: new insights into microsporidian genome dynamics and reductive evolution. PLoS Pathog 8: e1002979.
31. Hyun DW, Shin NR, Kim MS, Kim PS, Jung MJ, Kim JY et al. (2014). Polaribacter atrinae sp. nov., isolated from the intestine of a comb pen shell, Atrina pectinata. Int J Syst Evol Microbiol 64: 1654-1661.
32. Ishida T, Fushinobu S, Kawai R, Kitaoka M, Igarashi K, Samejima M. (2009). Crystal structure of glycoside hydrolase family 55 b-1,3-glucanase from the basidiomycete Phanerochaete chrysosporium. J Biol Chem 284: 10100-10109.
33. Kabisch A, Otto A, König S, Becher D, Albrecht D, Schuler M et al. (2014). Functional characterization of polysaccharide utilization loci in the marine Bacteroidetes 'Gramella forsetii' KT0803. ISME J 8: 1492-1502.
34. Kim B-C, Oh HW, Kim H, Park D-S, Hong SG, Lee HK et al. (2013). Polaribacter sejongensis sp. nov., isolated from Antarctic soil, and emended descriptions of the genus Polaribacter, Polaribacter butkevichii and Polaribacter irgensii. Int J Syst Evol Microbiol 63: 4000-4005.
35. Kimura H, Young CR, Martinez A, DeLong EF. (2011). Light-induced transcriptional responses associated with proteorhodopsin-enhanced growth in a marine flavobacterium. ISME J 5: 1641-1651.
36. Kirchman DL. (2000). Uptake and regeneration of inorganic nutrients by marine heterotrophic bacteria. In: Kirchman DL (ed). Microbial Ecology of the Oceans. Wiley-Liss: Hoboken, NJ, USA, pp 261-288.
37. Korth F, Deutsch B, Liskow I, Voss M. (2012). Uptake of dissolved organic nitrogen by size-fractionated plankton along a salinity gradient from the North Sea to the Baltic Sea. Biogeochemistry 111: 347-360.
38. Labourel A, Jam M, Jeudy A, Hehemann JH, Czjzek M, Michel G. (2014). The beta-glucanase ZgLamA from Zobellia galactanivorans evolved a bent active site adapted for efficient degradation of algal laminarin. J Biol Chem 289: 2027-2042.
39. Lami R, Cottrell MT, Campbell BJ, Kirchman DL. (2009). Light-dependent growth and proteorhodopsin expression by Flavobacteria and SAR11 in experiments with Delaware coastal waters. Environ Microbiol 11: 3201-3209.
40. Lee YS, Lee DH, Kahng HY, Jung JS. (2011). Polaribacter gangjinensis sp. nov., isolated from seawater. Int J Syst Evol Microbiol 61: 1425-1429.
41. Li H, Zhang XY, Liu C, Lin CY, Xu Z, Chen XL et al. (2014). Polaribacter huanghezhanensis sp. nov., isolated from Arctic fjord sediment, and emended description of the genus Polaribacter. Int J Syst Evol Microbiol 64: 973-978.
42. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. (2014). The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42: D490-D495.
43. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
44. Man D, Wang W, Sabehi G, Aravind L, Post AF, Massana R et al. (2003). Diversification and spectral tuning in marine proteorhodopsins. EMBO J 22: 1725-1731.
45. Mann AJ, Hahnke RL, Huang S, Werner J, Xing P, Barbeyron T et al. (2013). The genome of the algaassociated marine flavobacterium Formosa agariphila KMM 3901T reveals a broad potential for degradation of algal polysaccharides. Appl Environ Microbiol 79: 6813-6822.
46. Nedashkovskaya O, Kim S, Lysenko A, Kalinovskaya N, Mikhailov V, Kim I et al. (2005). Polaribacter butkevichii sp. nov., a novel marine mesophilic bacterium of the family Flavobacteriaceae. Curr Microbiol 51: 408-412.
47. Nedashkovskaya OI, Kim SB, Vancanneyt M, Snauwaert C, Lysenko AM, Rohde M et al. (2006). Formosa agariphila sp. nov., a budding bacterium of the family Flavobacteriaceae isolated from marine environments, and emended description of the genus Formosa. Int J Syst Evol Microbiol 56: 161-167.
48. Nedashkovskaya O, Kukhlevskiy A, Zhukova N. (2013). Polaribacter reichenbachii sp. nov.: a new marine bacterium associated with the green alga Ulva fenestrata. Curr Microbiol 66: 16-21.
49. Oh C, Heo S-J, De Zoysa M, Affan A, Jung W-K, Park H-S et al. (2011a). Whole-genome sequence of the xylanase-producing Mesoflavibacter zeaxanthinifaciens strain S86. J Bacteriol 193: 5557.
50. Oh C, Kwon Y-K, Heo S-J, De Zoysa M, Affan A, Lee Yet al. (2011b). Complete genome sequence of strain S85, a novel member of the family Flavobacteriaceae. J Bacteriol 193: 6107.
51. Otto A, Bernhardt J, Meyer H, Schaffer M, Herbst FA, Siebourg J et al. (2010). Systems-wide temporal proteomic profiling in glucose-starved Bacillus subtilis. Nat Commun 1: 137.
52. Parte AC. (2014). LPSN-list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 42: D613-D616.
53. Poretsky RS, Hewson I, Sun S, Allen AE, Zehr JP, Moran MA. (2009). Comparative day/night metatranscriptomic analysis of microbial communities in the North Pacific subtropical gyre. Environ Microbiol 11: 1358-1375.
54. Pruesse E, Peplies J, Glöckner FO. (2012). SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28: 1823-1829.
55. Rawlings ND, Waller M, Barrett AJ, Bateman A. (2014). MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 42: D503-D509.
56. Read SM, Currie G, Bacic A. (1996). Analysis of the structural heterogeneity of laminarin by electrosprayionisation- mass spectrometry. Carbohydr Res 281: 187-201.
57. Richter M, Rosselló-Móra R. (2009). Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106: 19126-19131.
58. Riedel T, Tomasch J, Buchholz I, Jacobs J, Kollenberg M, Gerdts G et al. (2010). Constitutive expression of the proteorhodopsin gene by a Flavobacterium strain representative of the proteorhodopsin-producing microbial community in the North Sea. Appl Environ Microbiol 76: 3187-3197.
59. Sonnenburg ED, Zheng H, Joglekar P, Higginbottom SK, Firbank SJ, Bolam DN et al. (2010). Specificity of polysaccharide use in intestinal Bacteroides species determines diet-induced microbiota alterations. Cell 141: 1241-1252.
60. Stamatakis A, Ott M. (2008). Efficient computation of the phylogenetic likelihood function on multi-gene alignments and multi-core architectures. Philos Trans R Soc Lond B Biol Sci 363: 3977-3984.
61. Steck E, Bräun J, Pelttari K, Kadel S, Kalbacher H, Richter W. (2007). Chondrocyte secreted CRTAC1: a glycosylated extracellular matrix molecule of human articular cartilage. Matrix Biol 26: 30-41.
62. Steindler L, Schwalbach MS, Smith DP, Chan F, Giovannoni SJ. (2011). Energy starved Candidatus Pelagibacter ubique substitutes light-mediated ATP production for endogenous carbon respiration. PLoS One 6: e19725.
63. Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM et al. (2012). Substratecontrolled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336: 608-611.
64. Thomas F, Hehemann JH, Rebuffet E, Czjzek M, Michel G. (2011). Environmental and gut Bacteroidetes: the food connection. Front Microbiol 2: 93.
65. Williams TJ, Wilkins D, Long E, Evans F, DeMaere MZ, Raftery MJ et al. (2013). The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics. Environ Microbiol 15: 1302-1317.
66. Woyke T, Xie G, Copeland A, González JM, Han C, Kiss H et al. (2009). Assembling the marine metagenome, one cell at a time. PLoS One 4: e5299.
67. Yarza P, Ludwig W, Euzéby J, Amann R, Schleifer KH, Glöckner FO et al. (2010). Update of the All- Species Living Tree Project based on 16S and 23S rRNA sequence analyses. Syst Appl Microbiol 33: 291-299.
68. Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y. (2012). dbCAN: a web resource for automated carbohydrateactive enzyme annotation. Nucleic Acids Res 40: W445-W451.
69. Yoon J-H, Kang S-J, Oh T-K. (2006). Polaribacter dokdonensis sp. nov., isolated from seawater. Int J Syst Evol Microbiol 56: 1251-1255.
70. Yoshizawa S, Kawanabe A, Ito H, Kandori H, Kogure K. (2012). Diversity and functional analysis of proteorhodopsin in marine Flavobacteria. Environ Microbiol 14: 1240-1248.
71. Yoshizawa S, Kumagai Y, Kim H, Ogura Y, Hayashi T, Iwasaki Wet al. (2014). Functional characterization of flavobacteria rhodopsins reveals a unique class of light-driven chloride pump in bacteria. Proc Natl Acad Sci USA 111: 6732-6737.
72. Zhang S, Xu C, Santschi PH. (2008). Chemical composition and 234Th (IV) binding of extracellular polymeric substances (EPS) produced by the marine diatom Amphora sp. Mar Chem 112: 81-92.
73. Zhou J, Bruns MA, Tiedje JM. (1996). DNA recovery from soils of diverse composition. Appl Environ Microbiol 62: 316-322.
74. Zhu Y, Suits MDL, Thompson AJ, Chavan S, Dinev Z, Dumon C et al. (2010). Mechanistic insights into a Ca2+-dependent family of a-mannosidases in a human gut symbiont. Nat Chem Biol 6: 125-132.
75. Zybailov B, Mosley AL, Sardiu ME, Coleman MK, Florens L, Washburn MP. (2006). Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J Proteome Res 5: 2339-2347.