Genomic and physiological analyses of ‘Reinekea forsetii’ reveal a versatile opportunistic lifestyle during spring algae blooms

Avcı B, Hahnke RL, Chafee M, Fischer T, Gruber-Vodicka H, Tegetmeyer H, Harder J, Fuchs BM, Amann RI, Teeling H (2016)
Environmental Microbiology 19(3): 1209-1221.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Autor*in
Avcı, Burak; Hahnke, Richard L.; Chafee, Meghan; Fischer, Tanja; Gruber-Vodicka, Harald; Tegetmeyer, HalinaUniBi ; Harder, Jens; Fuchs, Bernhard M.; Amann, Rudolf I.; Teeling, Hanno
Abstract / Bemerkung
Gammaproteobacterial Reinekea spp. were detected during North Sea spring algae blooms in the years 2009-2012, with relative abundances of up to 16% in the bacterioplankton. Here, we explore the ecophysiology of 'R. forsetii' strain Hel1_31_D35 that was isolated during the 2010 spring bloom using (i) its manually annotated, high-quality closed genome, (ii) re-analysis of in situ data from the 2009-2012 blooms and (iii) physiological tests. High resolution analysis of 16S rRNA gene sequences suggested that 'R. forsetii' dominated Reinekea populations during these blooms. This was corroborated by retrieval of almost complete Hel1_31_D35 genomes from 2009 and 2010 bacterioplankton metagenomes. Strain Hel1_31_D35 can use numerous low-molecular weight substrates including diverse sugar monomers, and few but relevant algal polysaccharides such as mannan, α-glucans, and likely bacterial peptidoglycan. It oxidizes thiosulfate to sulfate, and ferments under anoxic conditions. The strain can attach to algae and thrives at low phosphate concentrations as they occur during blooms. Its genome encodes RTX toxin and secretion proteins, and in cultivation experiments Hel1_31_D35 crude cell extracts inhibited growth of a North Sea Polaribacter strain. Our data suggest that the combination of these traits make strain Hel1_31_D35 a versatile opportunist that is particularly competitive during spring phytoplankton blooms.
Erscheinungsjahr
2016
Zeitschriftentitel
Environmental Microbiology
Band
19
Ausgabe
3
Seite(n)
1209-1221
ISSN
1462-2912
Page URI
https://pub.uni-bielefeld.de/record/2908401

Zitieren

Avcı B, Hahnke RL, Chafee M, et al. Genomic and physiological analyses of ‘Reinekea forsetii’ reveal a versatile opportunistic lifestyle during spring algae blooms. Environmental Microbiology. 2016;19(3):1209-1221.
Avcı, B., Hahnke, R. L., Chafee, M., Fischer, T., Gruber-Vodicka, H., Tegetmeyer, H., Harder, J., et al. (2016). Genomic and physiological analyses of ‘Reinekea forsetii’ reveal a versatile opportunistic lifestyle during spring algae blooms. Environmental Microbiology, 19(3), 1209-1221. doi:10.1111/1462-2920.13646
Avcı, Burak, Hahnke, Richard L., Chafee, Meghan, Fischer, Tanja, Gruber-Vodicka, Harald, Tegetmeyer, Halina, Harder, Jens, Fuchs, Bernhard M., Amann, Rudolf I., and Teeling, Hanno. 2016. “Genomic and physiological analyses of ‘Reinekea forsetii’ reveal a versatile opportunistic lifestyle during spring algae blooms”. Environmental Microbiology 19 (3): 1209-1221.
Avcı, B., Hahnke, R. L., Chafee, M., Fischer, T., Gruber-Vodicka, H., Tegetmeyer, H., Harder, J., Fuchs, B. M., Amann, R. I., and Teeling, H. (2016). Genomic and physiological analyses of ‘Reinekea forsetii’ reveal a versatile opportunistic lifestyle during spring algae blooms. Environmental Microbiology 19, 1209-1221.
Avcı, B., et al., 2016. Genomic and physiological analyses of ‘Reinekea forsetii’ reveal a versatile opportunistic lifestyle during spring algae blooms. Environmental Microbiology, 19(3), p 1209-1221.
B. Avcı, et al., “Genomic and physiological analyses of ‘Reinekea forsetii’ reveal a versatile opportunistic lifestyle during spring algae blooms”, Environmental Microbiology, vol. 19, 2016, pp. 1209-1221.
Avcı, B., Hahnke, R.L., Chafee, M., Fischer, T., Gruber-Vodicka, H., Tegetmeyer, H., Harder, J., Fuchs, B.M., Amann, R.I., Teeling, H.: Genomic and physiological analyses of ‘Reinekea forsetii’ reveal a versatile opportunistic lifestyle during spring algae blooms. Environmental Microbiology. 19, 1209-1221 (2016).
Avcı, Burak, Hahnke, Richard L., Chafee, Meghan, Fischer, Tanja, Gruber-Vodicka, Harald, Tegetmeyer, Halina, Harder, Jens, Fuchs, Bernhard M., Amann, Rudolf I., and Teeling, Hanno. “Genomic and physiological analyses of ‘Reinekea forsetii’ reveal a versatile opportunistic lifestyle during spring algae blooms”. Environmental Microbiology 19.3 (2016): 1209-1221.

1 Zitation in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Bacterial biofilm development during experimental degradation of Melicertus kerathurus exoskeleton in seawater.
Xaxiri NA, Nikouli E, Berillis P, Kormas KA., AIMS Microbiol 4(3), 2018
PMID: 31294223

63 References

Daten bereitgestellt von Europe PubMed Central.

Basic local alignment search tool.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ., J. Mol. Biol. 215(3), 1990
PMID: 2231712
Characterization of a novel family of fibronectin-binding proteins with M23 peptidase domains from Treponema denticola.
Bamford CV, Francescutti T, Cameron CE, Jenkinson HF, Dymock D., Mol Oral Microbiol 25(6), 2010
PMID: 21040511
SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing.
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA., J. Comput. Biol. 19(5), 2012
PMID: 22506599
Mapping glycoconjugate-mediated interactions of marine Bacteroidetes with diatoms.
Bennke CM, Neu TR, Fuchs BM, Amann R., Syst. Appl. Microbiol. 36(6), 2013
PMID: 23809997
The type VI secretion system of Vibrio cholerae fosters horizontal gene transfer.
Borgeaud S, Metzger LC, Scrignari T, Blokesch M., Science 347(6217), 2015
PMID: 25554784
Master recyclers: features and functions of bacteria associated with phytoplankton blooms.
Buchan A, LeCleir GR, Gulvik CA, Gonzalez JM., Nat. Rev. Microbiol. 12(10), 2014
PMID: 25134618
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics.
Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B., Nucleic Acids Res. 37(Database issue), 2008
PMID: 18838391
Carbohydrate-binding module tribes.
Carvalho CC, Phan NN, Chen Y, Reilly PJ., Biopolymers 103(4), 2015
PMID: 25381933
The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton.
Chiavelli DA, Marsh JW, Taylor RK., Appl. Environ. Microbiol. 67(7), 2001
PMID: 11425745
Variations in the substituted 3-linked mannans closely associated with the silicified walls of diatoms
Chiovitti, J. Phycol 41(), 2005
Reinekea aestuarii sp. nov., isolated from tidal flat sediment.
Choi A, Cho JC., Int. J. Syst. Evol. Microbiol. 60(Pt 12), 2010
PMID: 20081022
Composition and cycling of marine organic phosphorus
Clark, Limnol Oceanogr 46(), 2001
A mannose-sensitive haemagglutinin (MSHA)-like pilus promotes attachment of Pseudoalteromonas tunicata cells to the surface of the green alga Ulva australis.
Dalisay DS, Webb JS, Scheffel A, Svenson C, James S, Holmstrom C, Egan S, Kjelleberg S., Microbiology (Reading, Engl.) 152(Pt 10), 2006
PMID: 17005969
Minimum entropy decomposition: unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences.
Eren AM, Morrison HG, Lescault PJ, Reveillaud J, Vineis JH, Sogin ML., ISME J 9(4), 2015
PMID: 25325381
Biogeochemical Controls and Feedbacks on Ocean Primary Production
Falkowski PG, Barber RT, Smetacek V V., Science 281(5374), 1998
PMID: 9660741
Primary production of the biosphere: integrating terrestrial and oceanic components
Field CB, Behrenfeld MJ, Randerson JT, Falkowski P., Science 281(5374), 1998
PMID: 9657713
The Pfam protein families database.
Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A., Nucleic Acids Res. 38(Database issue), 2009
PMID: 19920124
Dilution cultivation of marine heterotrophic bacteria abundant after a spring phytoplankton bloom in the North Sea.
Hahnke RL, Bennke CM, Fuchs BM, Mann AJ, Rhiel E, Teeling H, Amann R, Harder J., Environ. Microbiol. 17(10), 2014
PMID: 24725270
Purification and characterization of β-Mannanase from Reinekea sp. KIT-YO10 with transglycosylation activity
Hakamada, Biosci, Biotechnol, Biochem 78(), 2014
Seagrass biofilm communities at a naturally CO2 -rich vent.
Hassenruck C, Hofmann LC, Bischof K, Ramette A., Environ Microbiol Rep 7(3), 2015
PMID: 25727314
Temporal and spatial constraints on community assembly during microbial colonization of wood in seawater.
Kalenitchenko D, Fagervold SK, Pruski AM, Vetion G, Yucel M, Le Bris N, Galand PE., ISME J 9(12), 2015
PMID: 25885564
Reinekea marina sp. nov., isolated from seawater, and emended description of the genus Reinekea.
Kang H, Kim H, Joung Y, Joh K., Int. J. Syst. Evol. Microbiol. 66(1), 2015
PMID: 26518601
Fast gapped-read alignment with Bowtie 2.
Langmead B, Salzberg SL., Nat. Methods 9(4), 2012
PMID: 22388286
The carbohydrate-active enzymes database (CAZy) in 2013.
Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B., Nucleic Acids Res. 42(Database issue), 2013
PMID: 24270786
Annual dynamics of North Sea bacterioplankton: seasonal variability superimposes short-term variation.
Lucas J, Wichels A, Teeling H, Chafee M, Scharfe M, Gerdts G., FEMS Microbiol. Ecol. 91(9), 2015
PMID: 26298013
ARB: a software environment for sequence data.
Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar , Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH., Nucleic Acids Res. 32(4), 2004
PMID: 14985472
The genome of the alga-associated marine flavobacterium Formosa agariphila KMM 3901T reveals a broad potential for degradation of algal polysaccharides.
Mann AJ, Hahnke RL, Huang S, Werner J, Xing P, Barbeyron T, Huettel B, Stuber K, Reinhardt R, Harder J, Glockner FO, Amann RI, Teeling H., Appl. Environ. Microbiol. 79(21), 2013
PMID: 23995932
Ecological genomics of marine Roseobacters.
Moran MA, Belas R, Schell MA, Gonzalez JM, Sun F, Sun S, Binder BJ, Edmonds J, Ye W, Orcutt B, Howard EC, Meile C, Palefsky W, Goesmann A, Ren Q, Paulsen I, Ulrich LE, Thompson LS, Saunders E, Buchan A., Appl. Environ. Microbiol. 73(14), 2007
PMID: 17526795
Production of carbohydrates by marine planktonic diatoms. I. Comparison of nine different species in culture
Myklestad, J Exp Mar Biol Ecol 15(), 1974
Genome characteristics of a generalist marine bacterial lineage.
Newton RJ, Griffin LE, Bowles KM, Meile C, Gifford S, Givens CE, Howard EC, King E, Oakley CA, Reisch CR, Rinta-Kanto JM, Sharma S, Sun S, Varaljay V, Vila-Costa M, Westrich JR, Moran MA., ISME J 4(6), 2010
PMID: 20072162
Phytoplankton community succession shaping bacterioplankton community composition in Lake Taihu, China.
Niu Y, Shen H, Chen J, Xie P, Yang X, Tao M, Ma Z, Qi M., Water Res. 45(14), 2011
PMID: 21684570
Reinekea blandensis sp. nov., a marine, genome-sequenced gammaproteobacterium.
Pinhassi J, Pujalte MJ, Macian MC, Lekunberri I, Gonzalez JM, Pedros-Alio C, Arahal DR., Int. J. Syst. Evol. Microbiol. 57(Pt 10), 2007
PMID: 17911313
SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes.
Pruesse E, Peplies J, Glockner FO., Bioinformatics 28(14), 2012
PMID: 22556368
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
Quast, Nucleic Acids Res (), 2013
The Genomes OnLine Database (GOLD) v.5: a metadata management system based on a four level (meta)genome project classification.
Reddy TB, Thomas AD, Stamatis D, Bertsch J, Isbandi M, Jansson J, Mallajosyula J, Pagani I, Lobos EA, Kyrpides NC., Nucleic Acids Res. 43(Database issue), 2014
PMID: 25348402
EMBOSS: the European Molecular Biology Open Software Suite.
Rice P, Longden I, Bleasby A., Trends Genet. 16(6), 2000
PMID: 10827456
Shifting the genomic gold standard for the prokaryotic species definition.
Richter M, Rossello-Mora R., Proc. Natl. Acad. Sci. U.S.A. 106(45), 2009
PMID: 19855009
The biochemistry and genetics of capsular polysaccharide production in bacteria
Roberts, Ann Rev Microbiol 50(), 1996
Reinekea marinisedimentorum gen. nov., sp. nov., a novel gammaproteobacterium from marine coastal sediments.
Romanenko LA, Schumann P, Rohde M, Mikhailov VV, Stackebrandt E., Int. J. Syst. Evol. Microbiol. 54(Pt 3), 2004
PMID: 15143005
Efficient computation of the phylogenetic likelihood function on multi-gene alignments and multi-core architectures.
Stamatakis A, Ott M., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 363(1512), 2008
PMID: 18852107
The SAR92 clade: an abundant coastal clade of culturable marine bacteria possessing proteorhodopsin.
Stingl U, Desiderio RA, Cho JC, Vergin KL, Giovannoni SJ., Appl. Environ. Microbiol. 73(7), 2007
PMID: 17293499
Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea.
Sowell SM, Wilhelm LJ, Norbeck AD, Lipton MS, Nicora CD, Barofsky DF, Carlson CA, Smith RD, Giovanonni SJ., ISME J 3(1), 2008
PMID: 18769456
Differing growth responses of major phylogenetic groups of marine bacteria to natural phytoplankton blooms in the western North Pacific Ocean.
Tada Y, Taniguchi A, Nagao I, Miki T, Uematsu M, Tsuda A, Hamasaki K., Appl. Environ. Microbiol. 77(12), 2011
PMID: 21515719
An association network analysis among microeukaryotes and bacterioplankton reveals algal bloom dynamics
Tan, J Phycol 5(), 2015
How family 26 glycoside hydrolases orchestrate catalysis on different polysaccharides: structure and activity of a Clostridium thermocellum lichenase, CtLic26A.
Taylor EJ, Goyal A, Guerreiro CI, Prates JA, Money VA, Ferry N, Morland C, Planas A, Macdonald JA, Stick RV, Gilbert HJ, Fontes CM, Davies GJ., J. Biol. Chem. 280(38), 2005
PMID: 15987675
Application of tetranucleotide frequencies for the assignment of genomic fragments.
Teeling H, Meyerdierks A, Bauer M, Amann R, Glockner FO., Environ. Microbiol. 6(9), 2004
PMID: 15305919
Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom.
Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, Kassabgy M, Huang S, Mann AJ, Waldmann J, Weber M, Klindworth A, Otto A, Lange J, Bernhardt J, Reinsch C, Hecker M, Peplies J, Bockelmann FD, Callies U, Gerdts G, Wichels A, Wiltshire KH, Glockner FO, Schweder T, Amann R., Science 336(6081), 2012
PMID: 22556258
Recurring patterns in bacterioplankton dynamics during coastal spring algae blooms.
Teeling H, Fuchs BM, Bennke CM, Kruger K, Chafee M, Kappelmann L, Reintjes G, Waldmann J, Quast C, Glockner FO, Lucas J, Wichels A, Gerdts G, Wiltshire KH, Amann RI., Elife 5(), 2016
PMID: 27054497

Thiele, 2011
Environmental and gut bacteroidetes: the food connection.
Thomas F, Hehemann JH, Rebuffet E, Czjzek M, Michel G., Front Microbiol 2(), 2011
PMID: 21747801

Tindall, 2007
Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement.
Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK, Earl AM., PLoS ONE 9(11), 2014
PMID: 25409509
Niches of two polysaccharide-degrading Polaribacter isolates from the North Sea during a spring diatom bloom.
Xing P, Hahnke RL, Unfried F, Markert S, Huang S, Barbeyron T, Harder J, Becher D, Schweder T, Glockner FO, Amann RI, Teeling H., ISME J 9(6), 2014
PMID: 25478683
Illumina sequencing-based analysis of free-living bacterial community dynamics during an Akashiwo sanguine bloom in Xiamen sea, China.
Yang C, Li Y, Zhou B, Zhou Y, Zheng W, Tian Y, Van Nostrand JD, Wu L, He Z, Zhou J, Zheng T., Sci Rep 5(), 2015
PMID: 25684124
dbCAN: a web resource for automated carbohydrate-active enzyme annotation.
Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y., Nucleic Acids Res. 40(Web Server issue), 2012
PMID: 22645317
Alkaliflexus imshenetskii gen. nov. sp. nov., a new alkaliphilic gliding carbohydrate-fermenting bacterium with propionate formation from a soda lake.
Zhilina TN, Appel R, Probian C, Brossa EL, Harder J, Widdel F, Zavarzin GA., Arch. Microbiol. 182(2-3), 2004
PMID: 15340778
DNA recovery from soils of diverse composition.
Zhou J, Bruns MA, Tiedje JM., Appl. Environ. Microbiol. 62(2), 1996
PMID: 8593035
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 28000419
PubMed | Europe PMC

Suchen in

Google Scholar