May 7, 2024
Chemotaxis shapes the microscale organization of the ocean’s microbiome – Nature

Chemotaxis shapes the microscale organization of the ocean’s microbiome – Nature

  • Azam, F. & Malfatti, F. Microbial structuring of marine ecosystems. Nat. Rev. Microbiol. 5, 782–791 (2007).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Blackburn, N., Fenchel, T. & Mitchell, J. Microscale nutrient patches in planktonic habitats shown by chemotactic bacteria. Science 282, 2254–2256 (1998).

    CAS 
    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Stocker, R. Marine microbes see a sea of gradients. Science 338, 628 (2012).

    CAS 
    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Levin, S. A. The problem of pattern and scale in ecology. Ecology 73, 1943–1967 (1992).

    Article 

    Google Scholar
     

  • Azam, F. Microbial control of oceanic carbon flux: the plot thickens. Science 280, 694–696 (1998).

    CAS 
    Article 

    Google Scholar
     

  • Strom, S. L. Microbial ecology of ocean biogeochemistry: a community perspective. Science 320, 1043–1045 (2008).

    CAS 
    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Sarmento, H. & Gasol, J. M. Use of phytoplankton-derived dissolved organic carbon by different types of bacterioplankton. Env. Microbiol. 14, 2348–2360 (2012).

    CAS 
    Article 

    Google Scholar
     

  • Grossart, H.-P., Riemann, L. & Azam, F. Bacterial motility in the sea and its ecological implications. Aquat. Microb. Ecol. 25, 247–258 (2001).

    Article 

    Google Scholar
     

  • Brumley, D. R. et al. Bacteria push the limits of chemotactic precision to navigate dynamic chemical gradients. Proc. Natl Acad. Sci. USA 116, 10792–10797 (2019).

    CAS 
    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fenchel, T. Eppur si muove: many water column bacteria are motile. Aquat. Microb. Ecol. 24, 197–201 (2001).

    Article 

    Google Scholar
     

  • Son, K., Menolascina, F. & Stocker, R. Speed-dependent chemotactic precision in marine bacteria. Proc. Natl Acad. Sci. USA 113, 8624–8629 (2016).

    CAS 
    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fenchel, T. Microbial behavior in a heterogeneous world. Science 296, 1068–1071 (2002).

    CAS 
    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Kiørboe, T. & Jackson, G. A. Marine snow, organic solute plumes, and optimal chemosensory behavior of bacteria. Limnol. Oceanogr. 46, 1309–1318 (2001).

    Article 
    ADS 

    Google Scholar
     

  • Lambert, B. S., Fernandez, V. I. & Stocker, R. Motility drives bacterial encounter with particles responsible for carbon export throughout the ocean. Limnol. Oceanogr. Lett. 4, 113–118 (2019).

    Article 

    Google Scholar
     

  • Wadhams, G. H. & Armitage, J. P. Making sense of it all: bacterial chemotaxis. Nat. Rev. Mol. Cell. Biol. 5, 1024–1037 (2004).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Stocker, R., Seymour, J. R., Samadani, A., Hunt, D. E. & Polz, M. F. Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches. Proc. Natl Acad. Sci. USA 105, 4209–4214 (2008).

    CAS 
    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Raina, J.-B., Fernandez, V., Lambert, B., Stocker, R. & Seymour, J. R. The role of microbial motility and chemotaxis in symbiosis. Nat. Rev. Microbiol. 17, 284–294 (2019).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Seymour, J. R., Amin, S. A., Raina, J.-B. & Stocker, R. Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships. Nat. Microbiol. 2, 17065 (2017).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Bell, W. & Mitchell, R. Chemotactic and growth responses of marine bacteria to algal extracellular products. Biol. Bull. 143, 265–277 (1972).

    Article 

    Google Scholar
     

  • Smriga, S., Fernandez, V. I., Mitchell, J. G. & Stocker, R. Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria. Proc. Natl Acad. Sci. USA 113, 1576–1581 (2016).

    CAS 
    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Amin, S. A. et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522, 98–101 (2015).

    CAS 
    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Lambert, B. S. et al. A microfluidics-based in situ chemotaxis assay to study the behaviour of aquatic microbial communities. Nat. Microbiol. 2, 1344–1349 (2017).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Larsen, M. H., Blackburn, N., Larsen, J. L. & Olsen, J. E. Influences of temperature, salinity and starvation on the motility and chemotactic response of Vibrio anguillarum. Microbiology 150, 1283–1290 (2004).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Rinke, C. et al. Validation of picogram- and femtogram-input DNA libraries for microscale metagenomics. PeerJ 4, e2486 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Becker, J. et al. Closely related phytoplankton species produce similar suites of dissolved organic matter. Front. Microbiol. 5, 111 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Vraspir, J. M. & Butler, A. Chemistry of marine ligands and siderophores. Annu. Rev. Mar. Sci. 1, 43–63 (2009).

    Article 
    ADS 

    Google Scholar
     

  • Tagliabue, A. et al. The integral role of iron in ocean biogeochemistry. Nature 543, 51–59 (2017).

    CAS 
    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Hopkinson, B. M. & Morel, F. M. M. The role of siderophores in iron acquisition by photosynthetic marine microorganisms. BioMetals 22, 659–669 (2009).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Amin, S. A. et al. Photolysis of iron–siderophore chelates promotes bacterial–algal mutualism. Proc. Natl Acad. Sci. USA 106, 17071–17076 (2009).

    CAS 
    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Croft, M. T., Lawrence, A. D., Raux-Deery, E., Warren, M. J. & Smith, A. G. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438, 90–93 (2005).

    CAS 
    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Helliwell, K. E. The roles of B vitamins in phytoplankton nutrition: new perspectives and prospects. New Phytol. 216, 62–68 (2017).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Berg, G. Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl. Microbiol. Biotechnol. 84, 11–18 (2009).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Christie, P. J., Whitaker, N. & González-Rivera, C. Mechanism and structure of the bacterial type IV secretion systems. Biochim. Biophys. Acta 1843, 1578–1591 (2014).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Preston, G. M. Metropolitan microbes: type III secretion in multihost symbionts. Cell Host Microbe 2, 291–294 (2007).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Deakin, W. J. & Broughton, W. J. Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat. Rev. Microbiol. 7, 312–320 (2009).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Luo, H. & Moran, M. A. Evolutionary ecology of the marine Roseobacter clade. Microbiol. Mol. Biol. Rev. 78, 573–587 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rolland, J. L., Stien, D., Sanchez-Ferandin, S. & Lami, R. Quorum sensing and quorum quenching in the phycosphere of phytoplankton: a case of chemical interactions in ecology. J. Chem. Ecol. 42, 1201–1211 (2016).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Fei, C. et al. Quorum sensing regulates ‘swim-or-stick’ lifestyle in the phycosphere. Environ. Microbiol. 22, 4761–4778 (2020).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Landa, M., Burns, A. S., Roth, S. J. & Moran, M. A. Bacterial transcriptome remodeling during sequential co-culture with a marine dinoflagellate and diatom. ISME J. 11, 2677 (2017).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rinke, C. et al. A phylogenomic and ecological analysis of the globally abundant Marine Group II archaea (Ca. Poseidoniales ord. nov.). ISME J. 13, 663–675 (2019).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Fenchel, T. & Blackburn, N. Motile chemosensory behaviour of phagotrophic protists: mechanisms for and efficiency in congregating at food patches. Protist 150, 325–336 (1999).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Hughes, D. J. et al. Impact of nitrogen availability upon the electron requirement for carbon fixation in Australian coastal phytoplankton communities. 63, 1891–1910 (2018).

  • Sumner, L. W. et al. Proposed minimum reporting standards for chemical analysis. Metabolomics 3, 211–221 (2007).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chong, J., Wishart, D. S. & Xia, J. Using MetaboAnalyst 4.0 for comprehensive and integrative metabolomics data analysis. Curr. Protoc. Bioinformatics 68, e86 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Xia, J. & Wishart, D. S. Web-based inference of biological patterns, functions and pathways from metabolomic data using MetaboAnalyst. Nat. Protoc. 6, 743–760 (2011).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Lambert, B. S. & Raina, J.-B. Fabrication and deployment of the in situ chemotaxis assay (ISCA). protocols.io https://doi.org/10.17504/protocols.io.kztcx6n (2019).

  • Ritchie, R. J. Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth. Res. 89, 27–41 (2006).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Marie, D., Partensky, F., Jacquet, S. & Vaulot, D. Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl. Environ. Microbiol. 63, 186–193 (1997).

    CAS 
    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bramucci, A. R. et al. Microvolume DNA extraction methods for microscale amplicon and metagenomic studies. ISME Commun. 1, 79 (2021).

    Article 

    Google Scholar
     

  • Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://doi.org/10.48550/arXiv.1303.3997 (2013).

  • Boyd, J. A., Woodcroft, B. J. & Tyson, G. W. GraftM: a tool for scalable, phylogenetically informed classification of genes within metagenomes. Nucleic Acids Res. 46, e59 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kuever, J., Rainey, F. A. & Widdel, F. In Bergey’s Manual of Systematics of Archaea and Bacteria https://doi.org/10.1002/9781118960608.obm00084 (2015).

  • Bianchi, D., Weber, T. S., Kiko, R. & Deutsch, C. Global niche of marine anaerobic metabolisms expanded by particle microenvironments. Nat. Geosci. 11, 263–268 (2018).

    CAS 
    Article 
    ADS 

    Google Scholar
     

  • Liu, X. et al. Wide distribution of anaerobic ammonium-oxidizing bacteria in the water column of the South China Sea: implications for their survival strategies. Divers. Distrib. 27, 1893–19003 (2021).

    Article 

    Google Scholar
     

  • Parks, D. H. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36, 996–1004 (2018).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Suzek, B. E., Huang, H., McGarvey, P., Mazumder, R. & Wu, C. H. UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23, 1282–1288 (2007).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Kanehisa, M. & Goto, S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 28, 27–30 (2000).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Paulson, J. N., Stine, O. C., Bravo, H. C. & Pop, M. Differential abundance analysis for microbial marker-gene surveys. Nat. Methods 10, 1200 (2013).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • McMurdie, P. J. & Holmes, S. Waste not, want not: why rarefying microbiome data is inadmissible. PLOS Comput. Biol. 10, e1003531 (2014).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Berges, J. A., Franklin, D. J. & Harrison, P. J. Evolution of an artificial seawater medium: improvements in enriched seawater, artificial water over the last two decades. J. Phycol. 37, 1138–1145 (2001).

    Article 

    Google Scholar
     

  • Lane, D. In Nucleic Acid Techniques in Bacterial Systematics (eds Stackebrandt, E. & Goodfellow, M.) 115–175 (1991).

  • Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods 13, 581–583 (2016).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Oksanen, J. et al. Package ‘Vegan’ Community Ecology Package Version 2 (2013).

  • Durham, B. P. et al. Sulfonate-based networks between eukaryotic phytoplankton and heterotrophic bacteria in the surface ocean. Nat. Microbiol. 4, 1706–1715 (2019).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Durham, B. P. et al. Recognition cascade and metabolite transfer in a marine bacteria–phytoplankton model system. Environ. Microbiol. 19, 3500–3513 (2017).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • Durham, B. P. et al. Cryptic carbon and sulfur cycling between surface ocean plankton. Proc. Natl Acad. Sci. USA 112, 453–457 (2015).

    CAS 
    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Landa, M. et al. Sulfur metabolites that facilitate oceanic phytoplankton–bacteria carbon flux. ISME J. 13, 2536–2550 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Source link