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Changing expression patterns of TonB-dependent transporters suggest shifts in polysaccharide consumption over the course of a spring phytoplankton bloom

  • 1.

    Behrenfeld MJ, Randerson JT, McClain CR, Feldman GC, Los SO, Tucker CJ, et al. Biospheric primary production during an ENSO transition. Science. 2001;291:2594–7.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 2.

    Buchan A, LeCleir GR, Gulvik CA, González JM. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol. 2014;12:686–98.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 3.

    Field CB, Behrenfeld MJ, Randerson JT, Falkowski P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science. 1998;281:237–40.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 4.

    Needham DM, Fuhrman JA. Pronounced daily succession of phytoplankton, archaea and bacteria following a spring bloom. Nat Microbiol. 2016;1:16005.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 5.

    Teeling H, Fuchs BM, Bennke CM, Krüger K, Chafee M, Kappelmann L, et al. Recurring patterns in bacterioplankton dynamics during coastal spring algae blooms. eLife. 2016;5:e11888.

    PubMed  PubMed Central  Article  Google Scholar 

  • 6.

    Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, et al. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science. 2012;336:608–11.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 7.

    Williams TJ, Wilkins D, Long E, Evans F, DeMaere MZ, Raftery MJ, et al. The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics. Environ Microbiol. 2013;15:1302–17.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 8.

    Chafee M, Fernàndez-Guerra A, Buttigieg PL, Gerdts G, Eren AM, Teeling H, et al. Recurrent patterns of microdiversity in a temperate coastal marine environment. ISME J. 2018;12:237–52.

    PubMed  Article  PubMed Central  Google Scholar 

  • 9.

    Francis TB, Krüger K, Fuchs BM, Teeling H, Amann RI. CandidatusProsiliicoccus vernus, a spring phytoplankton bloom associated member of the Flavobacteriaceae. Syst Appl Microbiol. 2019;42:41–53.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 10.

    Krüger K, Chafee M, Francis TB, Glavina del Rio T, Becher D, Schweder T, et al. In marine Bacteroidetes the bulk of glycan degradation during algae blooms is mediated by few clades using a restricted set of genes. ISME J. 2019;13:2800–16.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 11.

    Needham DM, Fichot EB, Wang E, Berdjeb L, Cram JA, Fichot CG, et al. Dynamics and interactions of highly resolved marine plankton via automated high-frequency sampling. ISME J. 2018;12:2417–32.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 12.

    Cottrell MT, Kirchman DL. Natural assemblages of marine Proteobacteria and members of the CytophagaFlavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microbiol. 2000;66:1692–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 13.

    Fernández-Gomez B, Richter M, Schüler M, Pinhassi J, Acinas SG, González JM, et al. Ecology of marine Bacteroidetes: a comparative genomics approach. ISME J. 2013;7:1026–37.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 14.

    Grondin JM, Tamura K, Déjean G, Abbott DW, Brumer H. Polysaccharide utilization loci: fueling microbial communities. J Bacteriol. 2017;199:e00860–16.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 15.

    Kappelmann L, Krüger K, Hehemann J-H, Harder J, Markert S, Unfried F, et al. Polysaccharide utilization loci of North Sea Flavobacteriia as basis for using SusC/D-protein expression for predicting major phytoplankton glycans. ISME J. 2019;13:76–91.

    CAS  PubMed  Article  Google Scholar 

  • 16.

    Kirchman DL. The ecology of CytophagaFlavobacteria in aquatic environments. FEMS Microbiol Ecol. 2002;39:91–100.

    CAS  PubMed  Google Scholar 

  • 17.

    Thomas F, Hehemann J-H, Rebuffet E, Czjzek M, Michel G. Environmental and gut Bacteroidetes: the food connection. Front Microbiol. 2011;2:93–93.

    PubMed  PubMed Central  Article  Google Scholar 

  • 18.

    Glenwright AJ, Pothula KR, Bhamidimarri SP, Chorev DS, Baslé A, Firbank SJ, et al. Structural basis for nutrient acquisition by dominant members of the human gut microbiota. Nature. 2017;541:407–11.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 19.

    Joglekar P, Sonnenburg ED, Higginbottom SK, Earle KA, Morland C, Shapiro-Ward S, et al. Genetic variation of the SusC/SusD homologs from a polysaccharide utilization locus underlies divergent fructan specificities and functional adaptation in Bacteroides thetaiotaomicron strains. mSphere. 2018;3:e00185–18.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 20.

    Cuskin F, Lowe EC, Temple MJ, Zhu Y, Cameron EA, Pudlo NA, et al. Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature. 2015;517:165–9.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 21.

    Reintjes G, Arnosti C, Fuchs BM, Amann R. An alternative polysaccharide uptake mechanism of marine bacteria. ISME J. 2017;11:1640–50.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 22.

    Hehemann J-H, Truong LV, Unfried F, Welsch N, Kabisch J, Heiden SE, et al. Aquatic adaptation of a laterally acquired pectin degradation pathway in marine Gammaproteobacteria. Environ Microbiol. 2017;19:2320–33.

    CAS  PubMed  Article  Google Scholar 

  • 23.

    Neumann AM, Balmonte JP, Berger M, Giebel H-A, Arnosti C, Voget S, et al. Different utilization of alginate and other algal polysaccharides by marine Alteromonas macleodii ecotypes. Environ Microbiol. 2015;17:3857–68.

    CAS  PubMed  Article  Google Scholar 

  • 24.

    Mirus O, Strauss S, Nicolaisen K, von Haeseler A, Schleiff E. TonB-dependent transporters and their occurrence in Cyanobacteria. BMC Biol. 2009;7:68.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 25.

    Gudmundsdottir A, Bell PE, Lundrigan MD, Bradbeer C, Kadner RJ. Point mutations in a conserved region (TonB box) of Escherichia coli outer membrane protein BtuB affect vitamin B12 transport. J Bacteriol. 1989;171:6526–33.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 26.

    Köster W, Braun V. Iron (III) hydroxamate transport into Escherichia coli. Substrate binding to the periplasmic FhuD protein. J Biol Chem. 1990;265:21407–10.

    PubMed  Article  Google Scholar 

  • 27.

    Schauer K, Gouget B, Carrière M, Labigne A, Reuse HD. Novel nickel transport mechanism across the bacterial outer membrane energized by the TonB/ExbB/ExbD machinery. Mol Microbiol. 2007;63:1054–68.

    CAS  PubMed  Article  Google Scholar 

  • 28.

    Reeves AR, D’Elia JN, Frias J, Salyers AA. A Bacteroides thetaiotaomicron outer membrane protein that is essential for utilization of maltooligosaccharides and starch. J Bacteriol. 1996;178:823–30.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 29.

    Cheng Q, Yu MC, Reeves AR, Salyers AA. Identification and characterization of a Bacteroides gene, csuF, which encodes an outer membrane protein that is essential for growth on chondroitin sulfate. J Bacteriol. 1995;177:3721–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 30.

    Neugebauer H, Herrmann C, Kammer W, Schwarz G, Nordheim A, Braun V. ExbBD-dependent transport of maltodextrins through the novel MalA protein across the outer membrane of Caulobacter crescentus. J Bacteriol. 2005;187:8300–11.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 31.

    Noinaj N, Guillier M, Barnard TJ, Buchanan SK. TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol. 2010;64:43–60.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 32.

    Schauer K, Rodionov DA, de Reuse H. New substrates for TonB-dependent transport: do we only see the ‘tip of the iceberg’? Trends Biochem Sci. 2008;33:330–8.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 33.

    Lapébie P, Lombard V, Drula E, Terrapon N, Henrissat B. Bacteroidetes use thousands of enzyme combinations to break down glycans. Nat Commun. 2019;10:2043.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 34.

    Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 2009;37:D233–8.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 35.

    Foley MH, Cockburn DW, Koropatkin NM. The Sus operon: a model system for starch uptake by the human gut Bacteroidetes. Cell Mol Life Sci. 2016;73:2603–17.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 36.

    Terrapon N, Lombard V, Gilbert HJ, Henrissat B. Automatic prediction of polysaccharide utilization loci in Bacteroidetes species. Bioinformatics. 2015;31:647–55.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 37.

    Terrapon N, Lombard V, Drula E, Lapébie P, Al-Masaudi S, Gilbert HJ, et al. PULDB: the expanded database of polysaccharide utilization loci. Nucleic Acids Res. 2017;46:D677–83.

    PubMed Central  Article  CAS  Google Scholar 

  • 38.

    Bergauer K, Fernandez-Guerra A, Garcia JA, Sprenger RR, Stepanauskas R, Pachiadaki MG, et al. Organic matter processing by microbial communities throughout the Atlantic water column as revealed by metaproteomics. Proc Natl Acad Sci USA. 2018;115:E400–8.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 39.

    Dong H-P, Hong Y-G, Lu S, Xie L-Y. Metaproteomics reveals the major microbial players and their biogeochemical functions in a productive coastal system in the northern South China Sea. Environ Microbiol Rep. 2014;6:683–95.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 40.

    McCarren J, Becker JW, Repeta DJ, Shi Y, Young CR, Malmstrom RR, et al. Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea. Proc Natl Acad Sci USA. 2010;107:16420–7.

    CAS  PubMed  Article  Google Scholar 

  • 41.

    Morris RM, Nunn BL, Frazar C, Goodlett DR, Ting YS, Rocap G. Comparative metaproteomics reveals ocean-scale shifts in microbial nutrient utilization and energy transduction. ISME J. 2010;4:673–85.

    CAS  PubMed  Article  Google Scholar 

  • 42.

    Williams TJ, Long E, Evans F, DeMaere MZ, Lauro FM, Raftery MJ, et al. A metaproteomic assessment of winter and summer bacterioplankton from Antarctic Peninsula coastal surface waters. ISME J. 2012;6:1883–900.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 43.

    Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. metaSPAdes: a new versatile metagenomic assembler. Genome Res. 2017;27:824–34.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 44.

    Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 2010;11:119.

    Article  CAS  Google Scholar 

  • 45.

    Besemer J, Lomsadze A, Borodovsky M. GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res. 2001;29:2607–18.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 46.

    Orellana LH, Francis TB, Krüger K, Teeling H, Müller M-C, Fuchs BM, et al. Niche differentiation among annually recurrent coastal Marine Group II Euryarchaeota. ISME J. 2019;13:3024–36.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 47.

    Eren AM, Esen ÖC, Quince C, Vineis JH, Morrison HG, Sogin ML, et al. Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ. 2015;3:e1319.

    PubMed  PubMed Central  Article  Google Scholar 

  • 48.

    Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 49.

    Deusch S, Seifert J. Catching the tip of the iceberg—evaluation of sample preparation protocols for metaproteomic studies of the rumen microbiota. Proteomics. 2015;15:3590–5.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 50.

    Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22:1658–9.

    CAS  PubMed  Article  Google Scholar 

  • 51.

    Nesvizhskii AI, Keller A, Kolker E, Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem. 2003;75:4646–58.

    CAS  PubMed  Article  Google Scholar 

  • 52.

    Florens L, Carozza MJ, Swanson SK, Fournier M, Coleman MK, Workman JL, et al. Analyzing chromatin remodeling complexes using shotgun proteomics and normalized spectral abundance factors. Methods. 2006;40:303–11.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 53.

    Perez-Riverol Y, Csordas A, Bai J, Bernal-Llinares M, Hewapathirana S, Kundu DJ, et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 2019;47:D442–50.

    CAS  PubMed  Article  Google Scholar 

  • 54.

    Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 55.

    Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH, Koren S, et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol. 2016;17:132.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 56.

    Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9.

    CAS  PubMed  Article  Google Scholar 

  • 57.

    Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil P-A, et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol. 2018;36:996–1004.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 58.

    Matsen FA, Kodner RB, Armbrust EV. pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinform. 2010;11:538.

    Article  Google Scholar 

  • 59.

    El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, et al. The Pfam protein families database in 2019. Nucleic Acids Res. 2019;47:D427–32.

    CAS  Article  Google Scholar 

  • 60.

    Saier MH, Reddy VS, Tsu BV, Ahmed MS, Li C, Moreno-Hagelsieb G. The Transporter Classification Database (TCDB): recent advances. Nucleic Acids Res. 2016;44:D372–9.

    CAS  PubMed  Article  Google Scholar 

  • 61.

    Eddy SR. Accelerated profile HMM searches. PLoS Comput Biol. 2011;7:e1002195.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 62.

    Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y. dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2012;40:W445–51.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 63.

    Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59–60.

    CAS  PubMed  Article  Google Scholar 

  • 64.

    Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2013;42:D490–5.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 65.

    Tang K, Jiao N, Liu K, Zhang Y, Li S. Distribution and functions of TonB-dependent transporters in marine bacteria and environments: implications for dissolved organic matter utilization. PLoS ONE. 2012;7:e41204.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 66.

    Gómez-Santos N, Glatter T, Koebnik R, Świątek-Połatyńska MA, Søgaard-Andersen L. A TonB-dependent transporter is required for secretion of protease PopC across the bacterial outer membrane. Nat Commun. 2019;10:1360.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 67.

    Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 68.

    Price MN, Dehal PS, Arkin AP. FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE. 2010;5:e9490.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 69.

    Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 2016;44:W242–5.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 70.

    Engel A, Händel N. A novel protocol for determining the concentration and composition of sugars in particulate and in high molecular weight dissolved organic matter (HMW-DOM) in seawater. Mar Chem. 2011;127:180–91.

    CAS  Article  Google Scholar 

  • 71.

    Reintjes G, Fuchs BM, Scharfe M, Wiltshire KH, Amann R, Arnosti C. Short-term changes in polysaccharide utilization mechanisms of marine bacterioplankton during a spring phytoplankton bloom. Environ Microbiol. 2020;22:1884–900.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 72.

    Avcı B, Krüger K, Fuchs BM, Teeling H, Amann RI. Polysaccharide niche partitioning of distinct Polaribacter clades during North Sea spring algal blooms. ISME J. 2020;14:1369–83.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 73.

    Sperling M, Piontek J, Engel A, Wiltshire KH, Niggemann J, Gerdts G, et al. Combined carbohydrates support rich communities of particle-associated marine bacterioplankton. Front Microbiol. 2017;8:65.

    PubMed  PubMed Central  Article  Google Scholar 

  • 74.

    Koch H, Dürwald A, Schweder T, Noriega-Ortega B, Vidal-Melgosa S, Hehemann J-H, et al. Biphasic cellular adaptations and ecological implications of Alteromonas macleodii degrading a mixture of algal polysaccharides. ISME J. 2019;13:92–103.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 75.

    Görke B, Stülke J. Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol. 2008;6:613–24.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 76.

    Becker S, Scheffel A, Polz MF, Hehemann J-H. Accurate quantification of laminarin in marine organic matter with enzymes from marine microbes. Appl Environ Microbiol. 2017;83:e03389–16.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 77.

    Becker S, Tebben J, Coffinet S, Wiltshire K, Iversen MH, Harder T, et al. Laminarin is a major molecule in the marine carbon cycle. Proc Natl Acad Sci USA. 2020;117:6599–607.

    CAS  PubMed  Article  PubMed Central  Google Scholar 


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