Syntrophic linkage between predatory Carpediemonas and specific prokaryotic populations

Hamann E, Tegetmeyer H, Riedel D, Littmann S, Ahmerkamp S, Chen J, Hach PF, Strous M (2017)
ISME JOURNAL 11(5): 1205-1217.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Autor*in
Hamann, Emmo; Tegetmeyer, HalinaUniBi ; Riedel, Dietmar; Littmann, Sten; Ahmerkamp, Soeren; Chen, Jianwei; Hach, Philipp F.; Strous, MarcUniBi
Abstract / Bemerkung
Most anoxic environments are populated by small (<10 mu m) heterotrophic eukaryotes that prey on different microbial community members. How predatory eukaryotes engage in beneficial interactions with other microbes has rarely been investigated so far. Here, we studied an example of such an interaction by cultivating the anerobic marine flagellate, Carpediemonas frisia sp. nov. (supergroup Excavata), with parts of its naturally associated microbiome. This microbiome consisted of so far uncultivated members of the Deltaproteobacteria, Bacteroidetes, Firmicutes, Verrucomicrobia and Nanoarchaeota. Using genome and transcriptome informed metabolic network modeling, we showed that Carpediemonas stimulated prokaryotic growth through the release of predigested biomolecules such as proteins, sugars, organic acids and hydrogen. Transcriptional gene activities suggested niche separation between biopolymer degrading Bacteroidetes, monomer utilizing Firmicutes and Nanoarchaeota and hydrogen oxidizing Deltaproteobacteria. An efficient metabolite exchange between the different community members appeared to be promoted by the formation of multispecies aggregates. Physiological experiments showed that Carpediemonas could also benefit from an association to these aggregates, as it facilitated the removal of inhibiting metabolites and increased the availability of prey bacteria. Taken together, our results provide a framework to understand how predatory microbial eukaryotes engage, across trophic levels, in beneficial interactions with specific prokaryotic populations.
Erscheinungsjahr
2017
Zeitschriftentitel
ISME JOURNAL
Band
11
Ausgabe
5
Seite(n)
1205-1217
ISSN
1751-7362
eISSN
1751-7370
Page URI
https://pub.uni-bielefeld.de/record/2911003

Zitieren

Hamann E, Tegetmeyer H, Riedel D, et al. Syntrophic linkage between predatory Carpediemonas and specific prokaryotic populations. ISME JOURNAL. 2017;11(5):1205-1217.
Hamann, E., Tegetmeyer, H., Riedel, D., Littmann, S., Ahmerkamp, S., Chen, J., Hach, P. F., et al. (2017). Syntrophic linkage between predatory Carpediemonas and specific prokaryotic populations. ISME JOURNAL, 11(5), 1205-1217. doi:10.1038/ismej.2016.197
Hamann, Emmo, Tegetmeyer, Halina, Riedel, Dietmar, Littmann, Sten, Ahmerkamp, Soeren, Chen, Jianwei, Hach, Philipp F., and Strous, Marc. 2017. “Syntrophic linkage between predatory Carpediemonas and specific prokaryotic populations”. ISME JOURNAL 11 (5): 1205-1217.
Hamann, E., Tegetmeyer, H., Riedel, D., Littmann, S., Ahmerkamp, S., Chen, J., Hach, P. F., and Strous, M. (2017). Syntrophic linkage between predatory Carpediemonas and specific prokaryotic populations. ISME JOURNAL 11, 1205-1217.
Hamann, E., et al., 2017. Syntrophic linkage between predatory Carpediemonas and specific prokaryotic populations. ISME JOURNAL, 11(5), p 1205-1217.
E. Hamann, et al., “Syntrophic linkage between predatory Carpediemonas and specific prokaryotic populations”, ISME JOURNAL, vol. 11, 2017, pp. 1205-1217.
Hamann, E., Tegetmeyer, H., Riedel, D., Littmann, S., Ahmerkamp, S., Chen, J., Hach, P.F., Strous, M.: Syntrophic linkage between predatory Carpediemonas and specific prokaryotic populations. ISME JOURNAL. 11, 1205-1217 (2017).
Hamann, Emmo, Tegetmeyer, Halina, Riedel, Dietmar, Littmann, Sten, Ahmerkamp, Soeren, Chen, Jianwei, Hach, Philipp F., and Strous, Marc. “Syntrophic linkage between predatory Carpediemonas and specific prokaryotic populations”. ISME JOURNAL 11.5 (2017): 1205-1217.

4 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Genomic diversity, lifestyles and evolutionary origins of DPANN archaea.
Dombrowski N, Lee JH, Williams TA, Offre P, Spang A., FEMS Microbiol Lett 366(2), 2019
PMID: 30629179
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
The draft genome of Kipferlia bialata reveals reductive genome evolution in fornicate parasites.
Tanifuji G, Takabayashi S, Kume K, Takagi M, Nakayama T, Kamikawa R, Inagaki Y, Hashimoto T., PLoS One 13(3), 2018
PMID: 29590215

49 References

Daten bereitgestellt von Europe PubMed Central.

SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing
AUTHOR UNKNOWN, 2012
Whole genome analysis of the marine Bacteroidetes'Gramella forsetii' reveals adaptations to degradation of polymeric organic matter.
Bauer M, Kube M, Teeling H, Richter M, Lombardot T, Allers E, Wurdemann CA, Quast C, Kuhl H, Knaust F, Woebken D, Bischof K, Mussmann M, Choudhuri JV, Meyer F, Reinhardt R, Amann RI, Glockner FO., Environ. Microbiol. 8(12), 2006
PMID: 17107561
Disruptive coloration and background pattern matching.
Cuthill IC, Stevens M, Sheppard J, Maddocks T, Parraga CA, Troscianko TS., Nature 434(7029), 2005
PMID: 15744301
Endosymbiotic methanogenic bacteria of the sapropelic amoeba Mastigella
AUTHOR UNKNOWN, 1985
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
Ubiquitous Gammaproteobacteria dominate dark carbon fixation in coastal sediments.
Dyksma S, Bischof K, Fuchs BM, Hoffmann K, Meier D, Meyerdierks A, Pjevac P, Probandt D, Richter M, Stepanauskas R, Mußmann M., ISME J 10(8), 2016
PMID: 26872043
Benthic eukaryotic diversity in the Guaymas Basin hydrothermal vent environment.
Edgcomb VP, Kysela DT, Teske A, de Vera Gomez A, Sogin ML., Proc. Natl. Acad. Sci. U.S.A. 99(11), 2002
PMID: 12032339
Locating proteins in the cell using TargetP, SignalP and related tools.
Emanuelsson O, Brunak S, von Heijne G, Nielsen H., Nat Protoc 2(4), 2007
PMID: 17446895
Ecology of marine Bacteroidetes: a comparative genomics approach.
Fernandez-Gomez B, Richter M, Schuler M, Pinhassi J, Acinas SG, Gonzalez JM, Pedros-Alio C., ISME J 7(5), 2013
PMID: 23303374

AUTHOR UNKNOWN, 1977
Pfam: the protein families database.
Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M., Nucleic Acids Res. 42(Database issue), 2013
PMID: 24288371
HMMER web server: 2015 update.
Finn RD, Clements J, Arndt W, Miller BL, Wheeler TJ, Schreiber F, Bateman A, Eddy SR., Nucleic Acids Res. 43(W1), 2015
PMID: 25943547
Prevalence and microdiversity of Alteromonas macleodii-like microorganisms in different oceanic regions.
Garcia-Martinez J, Acinas SG, Massana R, Rodriguez-Valera F., Environ. Microbiol. 4(1), 2002
PMID: 11966824
Using the metagenomics RAST server (MG-RAST) for analyzing shotgun metagenomes
AUTHOR UNKNOWN, 2010
Oxygen dynamics of marine sediments
AUTHOR UNKNOWN, 2008
Environmental Breviatea harbour mutualistic Arcobacter epibionts.
Hamann E, Gruber-Vodicka H, Kleiner M, Tegetmeyer HE, Riedel D, Littmann S, Chen J, Milucka J, Viehweger B, Becker KW, Dong X, Stairs CW, Hinrichs KU, Brown MW, Roger AJ, Strous M., Nature 534(7606), 2016
PMID: 27279223
Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates.
van Hoek AH, van Alen TA, Sprakel VS, Leunissen JA, Brigge T, Vogels GD, Hackstein JH., Mol. Biol. Evol. 17(2), 2000
PMID: 10677847
Enrichment of specific protozoan populations during in situ bioremediation of uranium-contaminated groundwater.
Holmes DE, Giloteaux L, Williams KH, Wrighton KC, Wilkins MJ, Thompson CA, Roper TJ, Long PE, Lovley DR., ISME J 7(7), 2013
PMID: 23446832
Gene finding in novel genomes.
Korf I., BMC Bioinformatics 5(), 2004
PMID: 15144565
NextClip: an analysis and read preparation tool for Nextera Long Mate Pair libraries.
Leggett RM, Clavijo BJ, Clissold L, Clark MD, Caccamo M., Bioinformatics 30(4), 2013
PMID: 24297520
SMART: recent updates, new developments and status in 2015.
Letunic I, Doerks T, Bork P., Nucleic Acids Res. 43(Database issue), 2014
PMID: 25300481
Diversity, stability and resilience of the human gut microbiota.
Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R., Nature 489(7415), 2012
PMID: 22972295
By-product inhibition effects on ethanolic fermentation by Saccharomyces cerevisiae.
Maiorella B, Blanch HW, Wilke CR., Biotechnol. Bioeng. 25(1), 1983
PMID: 18548541
Unveiling in situ interactions between marine protists and bacteria through single cell sequencing.
Martinez-Garcia M, Brazel D, Poulton NJ, Swan BK, Gomez ML, Masland D, Sieracki ME, Stepanauskas R., ISME J 6(3), 2011
PMID: 21938022
The genome of Syntrophus aciditrophicus: life at the thermodynamic limit of microbial growth.
McInerney MJ, Rohlin L, Mouttaki H, Kim U, Krupp RS, Rios-Hernandez L, Sieber J, Struchtemeyer CG, Bhattacharyya A, Campbell JW, Gunsalus RP., Proc. Natl. Acad. Sci. U.S.A. 104(18), 2007
PMID: 17442750
Biochemistry and evolution of anaerobic energy metabolism in eukaryotes.
Muller M, Mentel M, van Hellemond JJ, Henze K, Woehle C, Gould SB, Yu RY, van der Giezen M, Tielens AG, Martin WF., Microbiol. Mol. Biol. Rev. 76(2), 2012
PMID: 22688819
Acetogenesis from H2 plus CO2 and nitrogen fixation by an endosymbiotic spirochete of a termite-gut cellulolytic protist
AUTHOR UNKNOWN, 2015
Use of specific inhibitors in biogeochemistry and microbial ecology
AUTHOR UNKNOWN, 1988
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes.
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW., Genome Res. 25(7), 2015
PMID: 25977477
Energetics of syntrophic methane formation and the influence of aggregation
AUTHOR UNKNOWN, 1988
Significance of predation by protists in aquatic microbial food webs.
Sherr EB, Sherr BF., Antonie Van Leeuwenhoek 81(1-4), 2002
PMID: 12448728
Genomic insights into syntrophy: the paradigm for anaerobic metabolic cooperation.
Sieber JR, McInerney MJ, Gunsalus RP., Annu. Rev. Microbiol. 66(), 2012
PMID: 22803797
The ultrastructure of Carpediemonas membranifera (Eukaryota) with reference to the ‘excavate hypothesis’
AUTHOR UNKNOWN, 1999

AUTHOR UNKNOWN, 2013
Diversity and origins of anaerobic metabolism in mitochondria and related organelles
AUTHOR UNKNOWN, 2015
Electron transfer in syntrophic communities of anaerobic bacteria and archaea.
Stams AJ, Plugge CM., Nat. Rev. Microbiol. 7(8), 2009
PMID: 19609258
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
Multigene phylogenies of diverse Carpediemonas-like organisms identify the closest relatives of 'amitochondriate' diplomonads and retortamonads.
Takishita K, Kolisko M, Komatsuzaki H, Yabuki A, Inagaki Y, Cepicka I, Smejkalova P, Silberman JD, Hashimoto T, Roger AJ, Simpson AG., Protist 163(3), 2012
PMID: 22364773
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
The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism.
Waters E, Hohn MJ, Ahel I, Graham DE, Adams MD, Barnstead M, Beeson KY, Bibbs L, Bolanos R, Keller M, Kretz K, Lin X, Mathur E, Ni J, Podar M, Richardson T, Sutton GG, Simon M, Soll D, Stetter KO, Short JM, Noordewier M., Proc. Natl. Acad. Sci. U.S.A. 100(22), 2003
PMID: 14566062
Microbial ecology of expanding oxygen minimum zones.
Wright JJ, Konwar KM, Hallam SJ., Nat. Rev. Microbiol. 10(6), 2012
PMID: 22580367
Protist diversity in suboxic and sulfidic waters of the Black Sea.
Wylezich C, Jurgens K., Environ. Microbiol. 13(11), 2011
PMID: 21951296
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 28211847
PubMed | Europe PMC

Suchen in

Google Scholar