Chemotaxis shapes the microscale organization of the ocean’s microbiome
Azam, F. & Malfatti, F. Microbial structuring of marine ecosystems. Nat. Rev. Microbiol. 5, 782–791 (2007).CAS
Article
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
Google Scholar
Stocker, R. Marine microbes see a sea of gradients. Science 338, 628 (2012).CAS
Article
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
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
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
Google Scholar
Fenchel, T. Microbial behavior in a heterogeneous world. Science 296, 1068–1071 (2002).CAS
Article
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
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
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
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
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
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
Google Scholar
Amin, S. A. et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522, 98–101 (2015).CAS
Article
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
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
Google Scholar
Rinke, C. et al. Validation of picogram- and femtogram-input DNA libraries for microscale metagenomics. PeerJ 4, e2486 (2016).Article
Google Scholar
Becker, J. et al. Closely related phytoplankton species produce similar suites of dissolved organic matter. Front. Microbiol. 5, 111 (2014).Article
Google Scholar
Vraspir, J. M. & Butler, A. Chemistry of marine ligands and siderophores. Annu. Rev. Mar. Sci. 1, 43–63 (2009).Article
Google Scholar
Tagliabue, A. et al. The integral role of iron in ocean biogeochemistry. Nature 543, 51–59 (2017).CAS
Article
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
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
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
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
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
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
Google Scholar
Preston, G. M. Metropolitan microbes: type III secretion in multihost symbionts. Cell Host Microbe 2, 291–294 (2007).CAS
Article
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
Google Scholar
Luo, H. & Moran, M. A. Evolutionary ecology of the marine Roseobacter clade. Microbiol. Mol. Biol. Rev. 78, 573–587 (2014).Article
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
Google Scholar
Fei, C. et al. Quorum sensing regulates ‘swim-or-stick’ lifestyle in the phycosphere. Environ. Microbiol. 22, 4761–4778 (2020).CAS
Article
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
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
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
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
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
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
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
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
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
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
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
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
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
Google Scholar
Kanehisa, M. & Goto, S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 28, 27–30 (2000).CAS
Article
Google Scholar
Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59 (2014).Article
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
Google Scholar
McMurdie, P. J. & Holmes, S. Waste not, want not: why rarefying microbiome data is inadmissible. PLOS Comput. Biol. 10, e1003531 (2014).Article
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
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
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
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
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
Google Scholar
Landa, M. et al. Sulfur metabolites that facilitate oceanic phytoplankton–bacteria carbon flux. ISME J. 13, 2536–2550 (2019).CAS
Article
Google Scholar More