Microbial community structure affects marine dissolved organic matter composition

Frontiers in Marine Science

Volumn 3, Issue APR, 2016, Pages

  Kujawinski, Elizabeth B ^a   Longnecker, Krista ^a   Barott, Katie L ^a   Weber, Ralf J M ^b   Soule, Melissa C Kido ^a  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Bacteria; DOM; Microbial ecology; Peptides; Protozoa

Indexed keywords

EID: 85008627032     PISSN: None     EISSN: 22967745     Source Type: Journal    
DOI: 10.3389/fmars.2016.00045     Document Type: Article

References (72)

1. Allers, E., Gómez-Consarnau, L., Pinhassi, J., Gasol, J. M., Šimek, K., and Pernthaler, J. (2007). Response of Alteromonadaceae and Rhodobacteriaceae to glucose and phosphorus manipulation in marine mesocosms. Environ. Microbiol. 9, 2417-2429. doi: 10.1111/j.1462-2920.2007.01360.x
2. Alonso-Sáez, L., Sánchez, O., and Gasol, J. M. (2012). Bacterial uptake of low molecular weight organics in the subtropical Atlantic: are major phylogenetic groups functionally different? Limnol. Oceanogr. 57, 798-808. doi: 10.4319/lo.2012.57.3.0798
3. Alonso-Sáez, L., Unanue, M. A., Latatu, A., Azua, I., Ayo, B., Artolozaga, I., et al. (2009). Changes in marine prokaryotic community induced by varying types of dissolved organic matter and subsequent grazing pressure. J. Plankton Res. 31, 1373-1383. doi: 10.1093/plankt/fbp081
4. Amin, S. A., Parker, M. S., and Armbrust, E. V. (2012). Interactions between diatoms and bacteria. Microbiol. Mol. Biol. Rev. 76, 667-684. doi: 10.1128/MMBR.00007-12
5. Andersson, A., Lee, C., Azam, F., and Hagstrom, A. (1985). Release of amino acids and inorganic nutrients by heterotrophic marine microflagellates. Mar. Ecol. Prog. Ser. 23, 99-106. doi: 10.3354/meps023099
6. Arrieta, J. M., Mayol, E., Hansman, R. L., Herndl, G. J., Dittmar, T., and Duarte, C. M. (2015). Dilution limits dissolved organic carbon utilization in the deep ocean. Science 348, 331-333. doi: 10.1126/science.1258955
7. Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A., and Thingstad, F. (1983). The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257-263. doi: 10.3354/meps010257
8. Baltar, F., Palovaara, J., Unrein, F., Catala, P., Hornák, K., Šimek, K., et al. (2016). Marine bacterial community structure resilience to changes in protist predation under phytoplankton bloom conditions. ISME J. 10, 568-581. doi: 10.1038/ismej.2015.135
9. Baña, Z., Ayo, B., Marrasé, C., Gasol, J. M., and Iriberri, J. (2014). Changes in bacterial metabolism as a response to dissolved organic matter modification during protozoan grazing in coastal Canabrian and Mediterranean waters. Environ. Microbiol. 16, 498-511. doi: 10.1111/1462-2920.12274
10. Banning, E. C., Casciotti, K. L., and Kujawinski, E. B. (2010). Novel strains isolated from a coastal aquifer suggest a predatory role for Flavobacteria. FEMS Microbiol. Ecol. 73, 254-270. doi: 10.1111/j.1574-6941.2010.00897.x
11. Barbeau, K. A., Kujawinski, E. B., and Moffett, J. W. (2001). Remineralization and recycling of iron, thorium and organic carbon by heterotrophic marine protists in culture. Aquat. Microb. Ecol. 24, 69-81. doi: 10.3354/ame024069
12. Becker, J. W., Berube, P. M., Follett, C. L., Waterbury, J. B., Chisholm, S. W., DeLong, E. F., et al. (2014). Closely related phytoplankton species produce similar suites of dissolved organic matter. Front. Microbiol. 5:111. doi: 10.3389/fmicb.2014.00111
13. Bhatia, M. P., Das, S. B., Charette, M. A., Longnecker, K., and Kujawinski, E. B. (2010). Molecular characterization of dissolved organic matter associated with the Greenland ice sheet. Geochim. Cosmochim. Acta 74, 3768-3784. doi: 10.1016/j.gca.2010.03.035
14. Carlson, C. A. (2002). "Production and removal processes," in Biogeochemistry of Marine Dissolved Organic Matter, eds D. A. Hansell and C. A. Carlson (San Diego, CA: Elsevier Science), 91-152
15. Corno, G., and Jürgens, K. (2008). Structural and functional patterns of bacterial communities in response to protist predation along an experimental productivity gradient. Environ. Microbiol. 10, 2857-2871. doi: 10.1111/j.1462-2920.2008.01713.x
16. Cottrell, M. T., and Kirchman, D. L. (2000). Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low-and high-molecular-weight dissolved organic matter. Appl. Environ. Microbiol. 66, 1692-1697. doi: 10.1128/AEM.66.4.1692-1697.2000
17. Durham, B. P., Sharma, S., Luo, H., Smith, C. B., Amin, S. A., Bender, S. J., et al. (2015). Cryptic carbon and sulfur cycling between surface ocean plankton. Proc. Natl. Acad. Sci. U.S.A. 112, 453-457. doi: 10.1073/pnas.1413137112
18. Eiler, A., and Bertilsson, S. (2007). Flavobacteria blooms in four eutrophic lakes: Linking population dynamics of freshwater bacterioplankton to resource availability. Appl. Environ. Microbiol. 73, 3511-3518. doi: 10.1128/AEM.02534-06
19. Fouilland, E., Tolosa, I., Bonnet, D., Bouvier, C., Bouvier, T., Bouvy, M., et al. (2014). Bacterial carbon dependence on freshly produced phytoplankton exudates under different nutrient availability and grazing pressure conditions in coastal marine waters. FEMS Microbiol. Ecol. 87, 757-769. doi: 10.1111/1574-6941.12262
20. Gruber, D. F., Simjouw, J.-P., Seitzinger, S. P., and Taghon, G. L. (2006). Dynamics and characterization of refractory dissolved organic matter produced by a pure bacterial culture in an experimental predator-prey system. Appl. Environ. Microbiol. 72, 4184-4191. doi: 10.1128/AEM.02882-05
21. Hedges, J. I. (2002). "Why dissolved organics matter," in Biogeochemistry of Marine Dissolved Organic Matter, eds D. A. Hansell and C. A. Carlson (San Diego, CA: Elsevier Science), 1-34
22. Hertkorn, N., Benner, R., Frommberger, M., Schmitt-Kopplin, P., Witt, M., Kaiser, K., et al. (2006). Characterization of a major refractory component of marine dissolved organic matter. Geochim. Cosmochim. Acta 70, 2990-3010. doi: 10.1016/j.gca.2006.03.021
23. Hobbie, J. E., Daley, R. J., and Jasper, S. (1977). Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Appl. Environ. Microbiol. 33, 1225-1228
24. Horai, H., Arita, M., Kanaya, S., Nihei, Y., Ikeda, T., Suwa, K., et al. (2010). MassBank: a public repository for sharing mass spectral data for life sciences. J. Mass Spectrom. 45, 703-714. doi: 10.1002/jms.1777
25. Jiao, N., Herndl, G. J., Hansell, D. A., Benner, R., Kattner, G., Wilhelm, S. W., et al. (2010). Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat. Rev. Microbiol. 8, 593-599. doi: 10.1038/nrmicro2386
26. Jumars, P. A., Penry, D. L., Baross, J. A., Perry, M. J., and Frost, B. W. (1989). Closing the microbial loop: dissolved carbon pathway to heterotrophic bacteria from incomplete ingestion, digestion and absorption in animals. Deep Sea Res. 36, 483-495. doi: 10.1016/0198-0149(89)90001-0
27. Jürgens, K., and Massana, R. (2008). "Protistan grazing on marine bacterioplankton," in Microbial Ecology of the Oceans, ed D. L. Kirchman (New York, NY: Wiley), 383-441
28. Kaiser, K., and Benner, R. (2008). Major bacterial contribution to the ocean reservoir of detrital organic carbon and nitrogen. Limnol. Oceanogr. 53, 99-112. doi: 10.4319/lo.2008.53.1.0099
29. Kawasaki, N., and Benner, R. (2006). Bacterial release of dissolved organic matter during cell growth and decline: Molecular origin and composition. Limnol. Oceanogr. 51, 2170-2180. doi: 10.4319/lo.2006.51.5.2170
30. Kido Soule, M. C., Longnecker, K., Giovannoni, S. J., and Kujawinski, E. B. (2010). Impact of instrument and experimental parameters on the repeatability and reproducibility of peaks in ultrahigh resolution ESI FT-ICR mass spectra of natural organic matter. Org. Geochem. 41, 725-733. doi: 10.1016/j.orggeochem.2010.05.017
31. Kido Soule, M. C., Longnecker, K., Johnson, W. M., and Kujawinski, E. B. (2015). Environmental metabolomics: analytical strategies. Mar. Chem. 177, 374-387. doi: 10.1016/j.marchem.2015.06.029
32. Koch, B. P., Dittmar, T., Witt, M., and Kattner, G. (2007). Fundamentals of molecular formula assignment to ultrahigh resolution mass data of natural organic matter. Anal. Chem. 79, 1758-1763. doi: 10.1021/ac061949s
33. Kujawinski, E. B. (2011). The impact of microbial metabolism on marine dissolved organic matter. Ann. Rev. Mar. Sci. 3, 567-599. doi: 10.1146/annurev-marine-120308-081003
34. Kujawinski, E. B., and Behn, M. D. (2006). Automated analysis of electrospray ionization Fourier transform ion cyclotron resonance mass spectra of natural organic matter. Anal. Chem. 78, 4363-4373. doi: 10.1021/ac0600306
35. Kujawinski, E. B., Del Vecchio, R., Blough, N. V., Klein, G. C., and Marshall, A. G. (2004). Probing molecular-level transformations of dissolved organic matter: insights from electrospray ionization Fourier-transform ion cyclotron resonance mass spectrometry. Mar. Chem. 92, 23-37. doi: 10.1016/j.marchem.2004.06.038
36. Kujawinski, E. B., Longnecker, K., Blough, N. V., Del Vecchio, R., Finlay, L., Kitner, J. B., et al. (2009). Identification of possible source markers in marine dissolved organic matter using ultrahigh resolution electrospray ionization Fourier-transform ion cyclotron resonance mass spectrometry. Geochim. Cosmochim. Acta 73, 4384-4399. doi: 10.1016/j.gca.2009.04.033
37. Lechtenfeld, O. J., Hertkorn, N., Shen, Y., Witt, M., and Benner, R. (2015). Marine sequestration of carbon in bacterial metabolites. Nat. Commun. 6, 6711. doi: 10.1038/ncomms7711
38. Lima-Mendez, G., Faust, K., Henry, N., Decelle, J., Colin, S., Carcillo, F., et al. (2015). Determinants of community structure in the global plankton interactome. Science 348, 1262073. doi: 10.1126/science.1262073
39. Longnecker, K., Da Costa, A., Bhatia, M., and Kujawinski, E. B. (2009). Effect of carbon addition and predation on acetate-assimilating bacterial cells in groundwater. FEMS Microbiol. Ecol. 70, 456-470. doi: 10.1111/j.1574-6941.2009.00767.x
40. Longnecker, K., Futrelle, J., Coburn, E., Kido Soule, M. C., and Kujawinski, E. B. (2015a). Environmental metabolomics: databases and tools for data analysis. Mar. Chem. 177, 366-373. doi: 10.1016/j.marchem.2015.06.012
41. Longnecker, K., Kido Soule, M. C., and Kujawinski, E. B. (2015b). Dissolved organic matter produced by Thalassiosira pseudonana. Mar. Chem. 168, 114-123. doi: 10.1016/j.marchem.2014.11.003
42. Mantini, D., Petrucci, F., Pieragostino, D., Del Boccio, P., Di Nicola, M., Di Ilio, C., et al. (2007). LIMPIC: a computational method for the separation of protein MALDI-TOF-MS signals from noise. BMC Bioinformatics 8:101. doi: 10.1186/1471-2105-8-101
43. Matz, C., and Jürgens, K. (2003). Interaction of nutrient limitation and protozoan grazing determines the phenotypic structure of a bacterial community. Microb. Ecol. 45, 384-398. doi: 10.1007/s00248-003-2000-0
44. McCune, B., and Grace, J. (2002). Analysis of Ecological Communities. Gleneden Beach, OR: MjM Software Design
45. Mou, X. Z., Sun, S. L., Edwards, R. A., Hodson, R. E., and Moran, M. A. (2008). Bacterial carbon processing by generalist species in the coastal ocean. Nature 451, 708-U704. doi: 10.1038/nature06513
46. Nagata, T. (2000). "Production mechanisms of dissolved organic matter," in Microbial Ecology of the Oceans, 1st Edn., ed D. L. Kirchman (New York, NY: Wiley-Liss, Inc.), 121-152
47. Nagata, T., and Kirchman, D. L. (1991). Release of dissolved free and combined amino acids by bacterivorous marine flagellates. Limnol. Oceanogr. 36, 433-443. doi: 10.4319/lo.1991.36.3.0433
48. Nagata, T., and Kirchman, D. L. (1992). Release of macromolecular organic complexes by heterotrophic marine flagellates. Mar. Ecol. Prog. Ser. 83, 233-240. doi: 10.3354/meps083233
49. Ogawa, H., Amagai, Y., Koike, I., Kaiser, K., and Benner, R. (2001). Production of refractory dissolved organic matter by bacteria. Science 292, 917-920. doi: 10.1126/science.1057627
50. Osterholz, H., Niggemann, J., Giebel, H. A., Simon, M., and Dittmar, T. (2015). Inefficient microbial production of refractory dissolved organic matter in the ocean. Nat. Commun. 6, 7422. doi: 10.1038/ncomms8422
51. Passow, U. (2002). Production of transparent exopolymer particles (TEP) by phyto-and bacterioplankton. Mar. Ecol. Prog. Ser. 236, 1-12. doi: 10.3354/meps236001
52. Paul, C., Barofsky, A., Vidoudez, C., and Pohnert, G. (2009). Diatom exudates influence metabolism and cell growth of co-cultured diatom species. Mar. Ecol. Prog. Ser. 389, 61-79. doi: 10.3354/meps08162
53. Pedler Sherwood, B., Shaffer, E. A., Reyes, K., Longnecker, K., Aluwihare, L. I., and Azam, F. (2015). Metabolic characterization of a model heterotrophic bacterium capable of significant chemical alteration of marine dissolved organic matter. Mar. Chem. 177, 357-365. doi: 10.1016/j.marchem.2015.06.027
54. Pernthaler, J. (2005). Predation on prokaryotes in the water column and its ecological implications. Nat. Rev. Microbiol. 3, 537-546. doi: 10.1038/nrmicro1180
55. Rasche, F., Svatoš, A., Maddula, R. K., Böttcher, C., and Böcker, S. (2011). Computing fragmentation trees from tandem mass spectrometry data. Anal. Chem. 83, 1243-1251. doi: 10.1021/ac101825k
56. Santoro, A. E., and Casciotti, K. L. (2011). Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology and stable isotope fractionation. ISME J. 5, 1796-1808. doi: 10.1038/ismej.2011.58
57. Sarmento, H., Romera-Castillo, C., Lindh, M., Pinhassi, J., Sala, M. M., Gasol, J. M., et al. (2013). Phytoplankton species-specific release of dissolved free amino acids and their selective consumption by bacteria. Limnol. Oceanogr. 58, 1123-1135. doi: 10.4319/lo.2013.58.3.1123
58. Schleifer, K.-H., and Kandler, O. (1972). Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36, 407-477
59. Sher, D., Thompson, J. W., Kashtan, N., Croal, L., and Chisholm, S. W. (2011). Response of Prochlorococcus ecotypes to co-culture with diverse marine bacteria. ISME J. 5, 1125-1132. doi: 10.1038/ismej.2011.1
60. Sherr, E. B., and Sherr, B. F. (1994). Bacterivory and herbivory: key roles of phagotrophic protists in pelagic food webs. Microb. Ecol. 28, 223-235. doi: 10.1007/BF00166812
61. Sleighter, R. L., and Hatcher, P. G. (2008). Molecular characterization of dissolved organic matter (DOM) along a river to ocean transect of the lower Chesapeake Bay by ultrahigh resolution electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. Mar. Chem. 110, 140-152. doi: 10.1016/j.marchem.2008.04.008
62. Southam, A. D., Payne, T. G., Cooper, H. J., Arvanitis, T. N., and Viant, M. R. (2007). Dynamic range and mass accuracy of wide-scan direct infusion nanoelectrospray Fourier transform ion cyclotron resonance mass spectrometry-based metabolomics increased by the spectral stitching method. Anal. Chem. 79, 4595-4602. doi: 10.1021/ac062446p
63. Steinberg, D. K., Nelson, N. B., Carlson, C. A., and Prusak, A. C. (2004). Production of chromophoric dissolved organic matter (CDOM) in the open ocean by zooplankton and the colonial cyanobacterium Trichodesmium. Mar. Ecol. Prog. Ser. 267, 45-56. doi: 10.3354/meps267045
64. Stoderegger, K., and Herndl, G. J. (1998). Production and release of bacterial capsular material and its subsequent utilization by marine bacterioplankton. Limnol. Oceanogr. 43, 877-884. doi: 10.4319/lo.1998.43.5.0877
65. Strom, S. L., Benner, R., Ziegler, S., and Dagg, M. J. (1997). Planktonic grazers are a potentially important source of marine dissolved organic carbon. Limnol. Oceanogr. 42, 1364-1374. doi: 10.4319/lo.1997.42.6.1364
66. Tautenhahn, R., Cho, K., Uritboonthai, W., Zhu, Z., Patti, G. J., and Siuzdak, G. (2012). An accelerated workflow for untargeted metabolomics using the METLIN database. Nat. Biotechnol. 30, 826-828. doi: 10.1038/nbt.2348
67. Taylor, G., Iturriaga, R., and Sullivan, C. W. (1985). Interactions of bactivorous grazers and heterotrophic bacteria with dissolved organic matter. Mar. Ecol. Prog. Ser. 23, 129-141. doi: 10.3354/meps023129
68. Wang, H., Jiang, L., and Weitz, J. S. (2009). Bacterivorous grazers facilitate organic matter decomposition: a stoichiometric modeling approach. FEMS Microbiol. Ecol. 69, 170-179. doi: 10.1111/j.1574-6941.2009.00699.x
69. Watrous, J., Roach, P., Alexandrov, T., Heath, B. S., Yang, J. Y., Kersten, R. D., et al. (2012). Mass spectral molecular networking of living microbial colonies. Proc. Natl. Acad. Sci. U.S.A. 26, E1743-E1752. doi: 10.1073/pnas.1203689109
70. Weber, R. J. M., Selander, E., Sommer, U., and Viant, M. R. (2013). A stable-isotope mass spectrometry-based metabolic footprinting approach to analyze exudates from phytoplankton. Mar. Drugs 11, 4158-4175. doi: 10.3390/md11114158
71. Williams, D. K., and Muddiman, D. C. (2007). Parts-per-billion mass measurement accuracy achieved through the combination of multiple linear regression and automatic gain control in a Fourier transform ion cyclotron resonance mass spectrometer. Anal. Chem. 79, 5058-5063. doi: 10.1021/ac0704210
72. Wu, D., Hartman, A., Ward, N., and Eisen, J. A. (2008). An automated phylogenetic tree-based small subunit rRNA taxonomy and alignment pipeline (STAP). PLoS ONE 3:e2566. doi: 10.1371/annotation/c1aa88dd-4360-4902-8599-4d7edca79817