Environmental Breviatea harbour mutualistic Arcobacter epibionts

Hamann E, Gruber-Vodicka H, Kleiner M, Tegetmeyer H, Riedel D, Littmann S, Chen J, Milucka J, Viehweger B, Becker KW, Dong X, et al. (2016)
NATURE 534(7606): 254-258.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Hamann, Emmo; Gruber-Vodicka, Harald; Kleiner, Manuel; Tegetmeyer, HalinaUniBi ; Riedel, Dietmar; Littmann, Sten; Chen, Jianwei; Milucka, Jana; Viehweger, Bernhard; Becker, Kevin W.; Dong, Xiaoli; Stairs, Courtney W.
Abstract / Bemerkung
Breviatea form a lineage of free living, unicellular protists, distantly related to animals and fungi(1,2). This lineage emerged almost one billion years ago, when the oceanic oxygen content was low, and extant Breviatea have evolved or retained an anaerobic lifestyle(3,4). Here we report the cultivation of Lenisia limosa, gen. et sp. nov., a newly discovered breviate colonized by relatives of animal-associated Arcobacter. Physiological experiments show that the association of L. limosa with Arcobacter is driven by the transfer of hydrogen and is mutualistic, providing benefits to both partners. With whole-genome sequencing and differential proteomics, we show that an experimentally observed fitness gain of L. limosa could be explained by the activity of a so far unknown type of NAD(P) H-accepting hydrogenase, which is expressed in the presence, but not in the absence, of Arcobacter. Differential proteomics further reveal that the presence of Lenisia stimulates expression of known 'virulence' factors by Arcobacter. These proteins typically enable colonization of animal cells during infection(5), but may in the present case act for mutual benefit. Finally, re-investigation of two currently available transcriptomic data sets of other Breviatea(4) reveals the presence and activity of related hydrogen-consuming Arcobacter, indicating that mutualistic interaction between these two groups of microbes might be pervasive. Our results support the notion that molecular mechanisms involved in virulence can also support mutualism(6), as shown here for Arcobacter and Breviatea.
Page URI


Hamann E, Gruber-Vodicka H, Kleiner M, et al. Environmental Breviatea harbour mutualistic Arcobacter epibionts. NATURE. 2016;534(7606):254-258.
Hamann, E., Gruber-Vodicka, H., Kleiner, M., Tegetmeyer, H., Riedel, D., Littmann, S., Chen, J., et al. (2016). Environmental Breviatea harbour mutualistic Arcobacter epibionts. NATURE, 534(7606), 254-258. doi:10.1038/nature18297
Hamann, Emmo, Gruber-Vodicka, Harald, Kleiner, Manuel, Tegetmeyer, Halina, Riedel, Dietmar, Littmann, Sten, Chen, Jianwei, et al. 2016. “Environmental Breviatea harbour mutualistic Arcobacter epibionts”. NATURE 534 (7606): 254-258.
Hamann, E., Gruber-Vodicka, H., Kleiner, M., Tegetmeyer, H., Riedel, D., Littmann, S., Chen, J., Milucka, J., Viehweger, B., Becker, K. W., et al. (2016). Environmental Breviatea harbour mutualistic Arcobacter epibionts. NATURE 534, 254-258.
Hamann, E., et al., 2016. Environmental Breviatea harbour mutualistic Arcobacter epibionts. NATURE, 534(7606), p 254-258.
E. Hamann, et al., “Environmental Breviatea harbour mutualistic Arcobacter epibionts”, NATURE, vol. 534, 2016, pp. 254-258.
Hamann, E., Gruber-Vodicka, H., Kleiner, M., Tegetmeyer, H., Riedel, D., Littmann, S., Chen, J., Milucka, J., Viehweger, B., Becker, K.W., Dong, X., Stairs, C.W., Hinrichs, K.-U., Brown, M.W., Roger, A.J., Strous, M.: Environmental Breviatea harbour mutualistic Arcobacter epibionts. NATURE. 534, 254-258 (2016).
Hamann, Emmo, Gruber-Vodicka, Harald, Kleiner, Manuel, Tegetmeyer, Halina, Riedel, Dietmar, Littmann, Sten, Chen, Jianwei, Milucka, Jana, Viehweger, Bernhard, Becker, Kevin W., Dong, Xiaoli, Stairs, Courtney W., Hinrichs, Kai-Uwe, Brown, Matthew W., Roger, Andrew J., and Strous, Marc. “Environmental Breviatea harbour mutualistic Arcobacter epibionts”. NATURE 534.7606 (2016): 254-258.

15 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Diversity of opisthokont septin proteins reveals structural constraints and conserved motifs.
Auxier B, Dee J, Berbee ML, Momany M., BMC Evol Biol 19(1), 2019
PMID: 30616529
Biological composition and microbial dynamics of sinking particulate organic matter at abyssal depths in the oligotrophic open ocean.
Boeuf D, Edwards BR, Eppley JM, Hu SK, Poff KE, Romano AE, Caron DA, Karl DM, DeLong EF., Proc Natl Acad Sci U S A 116(24), 2019
PMID: 31127042
Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO2 Fixation.
Seah BKB, Antony CP, Huettel B, Zarzycki J, Schada von Borzyskowski L, Erb TJ, Kouris A, Kleiner M, Liebeke M, Dubilier N, Gruber-Vodicka HR., MBio 10(3), 2019
PMID: 31239380
Evidence for H2 consumption by uncultured Desulfobacterales in coastal sediments.
Dyksma S, Pjevac P, Ovanesov K, Mussmann M., Environ Microbiol 20(2), 2018
PMID: 28772023
Microbial eukaryotes have adapted to hypoxia by horizontal acquisitions of a gene involved in rhodoquinone biosynthesis.
Stairs CW, Eme L, Muñoz-Gómez SA, Cohen A, Dellaire G, Shepherd JN, Fawcett JP, Roger AJ., Elife 7(), 2018
PMID: 29697049
Farming, slaving and enslavement: histories of endosymbioses during kinetoplastid evolution.
Harmer J, Yurchenko V, Nenarokova A, Lukeš J, Ginger ML., Parasitology 145(10), 2018
PMID: 29895336
Syntrophic linkage between predatory Carpediemonas and specific prokaryotic populations.
Hamann E, Tegetmeyer HE, Riedel D, Littmann S, Ahmerkamp S, Chen J, Hach PF, Strous M., ISME J 11(5), 2017
PMID: 28211847
Symbiosis in eukaryotic evolution.
López-García P, Eme L, Moreira D., J Theor Biol 434(), 2017
PMID: 28254477
Short-chain alkanes fuel mussel and sponge Cycloclasticus symbionts from deep-sea gas and oil seeps.
Rubin-Blum M, Antony CP, Borowski C, Sayavedra L, Pape T, Sahling H, Bohrmann G, Kleiner M, Redmond MC, Valentine DL, Dubilier N., Nat Microbiol 2(), 2017
PMID: 28628098
Extreme genome diversity in the hyper-prevalent parasitic eukaryote Blastocystis.
Gentekaki E, Curtis BA, Stairs CW, Klimeš V, Eliáš M, Salas-Leiva DE, Herman EK, Eme L, Arias MC, Henrissat B, Hilliou F, Klute MJ, Suga H, Malik SB, Pightling AW, Kolisko M, Rachubinski RA, Schlacht A, Soanes DM, Tsaousis AD, Archibald JM, Ball SG, Dacks JB, Clark CG, van der Giezen M, Roger AJ., PLoS Biol 15(9), 2017
PMID: 28892507
Assessing species biomass contributions in microbial communities via metaproteomics.
Kleiner M, Thorson E, Sharp CE, Dong X, Liu D, Li C, Strous M., Nat Commun 8(1), 2017
PMID: 29146960
Bacterial Succession on Sinking Particles in the Ocean's Interior.
Pelve EA, Fontanez KM, DeLong EF., Front Microbiol 8(), 2017
PMID: 29225592
HydDB: A web tool for hydrogenase classification and analysis.
Søndergaard D, Pedersen CN, Greening C., Sci Rep 6(), 2016
PMID: 27670643

52 References

Daten bereitgestellt von Europe PubMed Central.

Earth history. Low mid-Proterozoic atmospheric oxygen levels and the delayed rise of animals.
Planavsky NJ, Reinhard CT, Wang X, Thomson D, McGoldrick P, Rainbird RH, Johnson T, Fischer WW, Lyons TW., Science 346(6209), 2014
PMID: 25359975
Estimating the timing of early eukaryotic diversification with multigene molecular clocks.
Parfrey LW, Lahr DJ, Knoll AH, Katz LA., Proc. Natl. Acad. Sci. U.S.A. 108(33), 2011
PMID: 21810989
Phylogenomics demonstrates that breviate flagellates are relatedto opisthokonts and apusomonads
Brown MW., 2013
A SUF Fe-S cluster biogenesis system in the mitochondrion-related organelles of the anaerobic protist Pygsuia.
Stairs CW, Eme L, Brown MW, Mutsaers C, Susko E, Dellaire G, Soanes DM, van der Giezen M, Roger AJ., Curr. Biol. 24(11), 2014
PMID: 24856215
Vulvovaginal candidiasis: Epidemiology, microbiology and risk factors.
Goncalves B, Ferreira C, Alves CT, Henriques M, Azeredo J, Silva S., Crit. Rev. Microbiol. 42(6), 2015
PMID: 26690853
Abundant toxin-related genes in the genomes of beneficial symbionts from deep-sea hydrothermal vent mussels.
Sayavedra L, Kleiner M, Ponnudurai R, Wetzel S, Pelletier E, Barbe V, Satoh N, Shoguchi E, Fink D, Breusing C, Reusch TB, Rosenstiel P, Schilhabel MB, Becher D, Schweder T, Markert S, Dubilier N, Petersen JM., Elife 4(), 2015
PMID: 26371554
Animals in a bacterial world, a new imperative for the life sciences.
McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Loso T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ., Proc. Natl. Acad. Sci. U.S.A. 110(9), 2013
PMID: 23391737
The Capsaspora genome reveals a complex unicellular prehistory of animals.
Suga H, Chen Z, de Mendoza A, Sebe-Pedros A, Brown MW, Kramer E, Carr M, Kerner P, Vervoort M, Sanchez-Pons N, Torruella G, Derelle R, Manning G, Lang BF, Russ C, Haas BJ, Roger AJ, Nusbaum C, Ruiz-Trillo I., Nat Commun 4(), 2013
PMID: 23942320
The Chlamydomonas genome reveals the evolution of key animal and plant functions.
Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR., Science 318(5848), 2007
PMID: 17932292
Diversity and origins of anaerobic metabolism in mitochondria and related organelles.
Stairs CW, Leger MM, Roger AJ., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 370(1678), 2015
PMID: 26323757
Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I.
Hrdy I, Hirt RP, Dolezal P, Bardonova L, Foster PG, Tachezy J, Embley TM., Nature 432(7017), 2004
PMID: 15577909
Electron transfer in syntrophic communities of anaerobic bacteria and archaea.
Stams AJ, Plugge CM., Nat. Rev. Microbiol. 7(8), 2009
PMID: 19609258
Active migration into the subcellular space precedes Campylobacter jejuni invasion of epithelial cells.
van Alphen LB, Bleumink-Pluym NM, Rochat KD, van Balkom BW, Wosten MM, van Putten JP., Cell. Microbiol. 10(1), 2008
PMID: 18052944
Using the metagenomics RAST server (MG-RAST) for analyzingshotgun metagenomes
Glass EM, Wilkening J, Wilke A, Antonopoulos D, Meyer F., 2010
Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria.
Pernthaler A, Pernthaler J, Amann R., Appl. Environ. Microbiol. 68(6), 2002
PMID: 12039771
Velvet: algorithms for de novo short read assembly using de Bruijn graphs.
Zerbino DR, Birney E., Genome Res. 18(5), 2008
PMID: 18349386
The binning of metagenomic contigs for microbial physiology of mixed cultures.
Strous M, Kraft B, Bisdorf R, Tegetmeyer HE., Front Microbiol 3(), 2012
PMID: 23227024
Fast gapped-read alignment with Bowtie 2.
Langmead B, Salzberg SL., Nat. Methods 9(4), 2012
PMID: 22388286
GapFiller: a de novo assembly approach to fill the gap withinpaired reads
Nadalin F, Vezzi F, Policriti A., 2012
MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes.
Cantarel BL, Korf I, Robb SM, Parra G, Ross E, Moore B, Holt C, Sanchez Alvarado A, Yandell M., Genome Res. 18(1), 2007
PMID: 18025269
Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training.
Ter-Hovhannisyan V, Lomsadze A, Chernoff YO, Borodovsky M., Genome Res. 18(12), 2008
PMID: 18757608
Gene finding in novel genomes.
Korf I., BMC Bioinformatics 5(), 2004
PMID: 15144565
Using RepeatMasker to identify repetitive elements in genomicsequences
Chen N., 2004
Phylogenomics demonstrates that breviate flagellates are relatedto opisthokonts and apusomonads
Brown MW., 2013
KEGG for integration and interpretation of large-scale moleculardata sets
Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M., 2012
Predicting subcellular localization of proteins based on their N-terminal amino acid sequence.
Emanuelsson O, Nielsen H, Brunak S, von Heijne G., J. Mol. Biol. 300(4), 2000
PMID: 10891285
MitoProt, a Macintosh application for studying mitochondrial proteins.
Claros MG., Comput. Appl. Biosci. 11(4), 1995
PMID: 8521054
HMMER web server: interactive sequence similarity searching.
Finn RD, Clements J, Eddy SR., Nucleic Acids Res. 39(Web Server issue), 2011
PMID: 21593126
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
SMART: recent updates, new developments and status in 2015.
Letunic I, Doerks T, Bork P., Nucleic Acids Res. 43(Database issue), 2014
PMID: 25300481
CheckM: assessing the quality of microbial genomes recovered fromisolates, single cells, and metagenomes Donovan
Donovan H, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW., 2014
Broadly sampled multigene analyses yield a well-resolved eukaryotic tree of life.
Parfrey LW, Grant J, Tekle YI, Lasek-Nesselquist E, Morrison HG, Sogin ML, Patterson DJ, Katz LA., Syst. Biol. 59(5), 2010
PMID: 20656852
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP., Syst. Biol. 61(3), 2012
PMID: 22357727
Universal sample preparation method for proteome analysis.
Wisniewski JR, Zougman A, Nagaraj N, Mann M., Nat. Methods 6(5), 2009
PMID: 19377485
Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap.
Olsen JV, de Godoy LM, Li G, Macek B, Mortensen P, Pesch R, Makarov A, Lange O, Horning S, Mann M., Mol. Cell Proteomics 4(12), 2005
PMID: 16249172
Improvements to the percolator algorithm for Peptide identification from shotgun proteomics data sets.
Spivak M, Weston J, Bottou L, Kall L, Noble WS., J. Proteome Res. 8(7), 2009
PMID: 19385687
Analyzing chromatin remodeling complexes using shotgun proteomics and normalized spectral abundance factors.
Florens L, Carozza MJ, Swanson SK, Fournier M, Coleman MK, Workman JL, Washburn MP., Methods 40(4), 2006
PMID: 17101441
Ecological distribution and population physiology defined by proteomics in a natural microbial community.
Mueller RS, Denef VJ, Kalnejais LH, Suttle KB, Thomas BC, Wilmes P, Smith RL, Nordstrom DK, McCleskey RB, Shah MB, Verberkmoes NC, Hettich RL, Banfield JF., Mol. Syst. Biol. 6(), 2010
PMID: 20531404
Significance analysis of microarrays applied to the ionizing radiation response.
Tusher VG, Tibshirani R, Chu G., Proc. Natl. Acad. Sci. U.S.A. 98(9), 2001
PMID: 11309499
SRAdb: query and use public next-generation sequencing data from within R.
Zhu Y, Stephens RM, Meltzer PS, Davis SR., BMC Bioinformatics 14(), 2013
PMID: 23323543
Fast and accurate long-read alignment with Burrows-Wheeler transform.
Li H, Durbin R., Bioinformatics 26(5), 2010
PMID: 20080505
Fast and sensitive protein alignment usingDIAMOND
Buchfink B, Xie C, Huson DH., 2015
Electron transfer in syntrophic communities of anaerobic bacteria and archaea.
Stams AJ, Plugge CM., Nat. Rev. Microbiol. 7(8), 2009
PMID: 19609258
Imaging cytosolic NADH-NAD(+) redox state with a genetically encoded fluorescent biosensor.
Hung YP, Albeck JG, Tantama M, Yellen G., Cell Metab. 14(4), 2011
PMID: 21982714

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

PMID: 27279223
PubMed | Europe PMC

Suchen in

Google Scholar