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Associated Bacterial Community Structures with the Growth of the Marine Centric Diatom Cyclotella meneghiniana: Evidence in Culture Stages

해양 원형 규조류 Cyclotella meneghiniana 성장 연관 미생물 군집구조 분석: 배양단계에 따른 증거

  • Choi, Won-Ji (Department of Biotechnology, Sangmyung University) ;
  • Park, Bum Soo (Department of Biotechnology, Sangmyung University) ;
  • Guo, Ruoyu (Department of Biotechnology, Sangmyung University) ;
  • Ki, Jang-Seu (Department of Biotechnology, Sangmyung University)
  • Received : 2017.08.22
  • Accepted : 2017.11.28
  • Published : 2017.12.30

Abstract

There are a number of pieces of evidences that suggest a link between marine diatoms and microorganisms, but knowledge about related microbial communities is greatly lacking. The present study investigated the microbial community structures related to the growth of the marine diatom Cyclotella meneghiniana. We collected free-living bacteria (FLB) and particle-associated bacteria (PAB) at each growth stage (e.g., lag, exponential, stationary and death) of the diatom, and analyzed their bacterial 16S rDNA using pyrosequencing. Metagenomics analysis showed that community structures of FLB and PAB differed considerably with the progress of growth stages. FLB showed higher diversity than PAB, but variation in the different growth stages of C. meneghiniana was more evident in PAB. The proportion of the genus Hoeflea, belonging to the order Rhizobiales, was dominant in both FLB and PAB, and it gradually increased with the growth of C. meneghiniana. However, Enhydrobacter clade tended to considerably decrease in PAB. In addition, Marinobacter decreased steadily in FLB, but first increased and then decreased in PAB. These results suggest that Hoeflea, Enhydrobacter, and Marinobacter may be closely related to the growth of diatom C. meneghiniana.

Keywords

References

  1. Amaro AM, Fuentes MS, Ogalde SR, Venegas JA, Suarez-Isla BA (2005) Identification and characterization of potentially algal-lytic marine bacteria strongly associated with the toxic dinoflagellate Alexandrium catenella. J Eukaryot Microbiol 52(3):191-200 https://doi.org/10.1111/j.1550-7408.2005.00031.x
  2. Amin SA, Green DH, Hart MC, Kupper FC, Sunda WG, Carrano CJ (2009) Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism. P Natl A Sci USA 106:17071-17076 https://doi.org/10.1073/pnas.0905512106
  3. Amin SA, Green DH, Al Waheeb D, Gardes A, Carrano CJ (2012) Iron transport in the genus Marinobacter. Biometals 25:135-147 https://doi.org/10.1007/s10534-011-9491-9
  4. Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Brzezinski MA (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79-86 https://doi.org/10.1126/science.1101156
  5. Ashen JB, Cohen JD, Goff LJ (1999) GC-SIM-MS detection and quantification of free indole-3-acetic acid bacterial galls on the marine alga Prionitis lanceolata (Rhodophyta). J Phycol 35:493-500 https://doi.org/10.1046/j.1529-8817.1999.3530493.x
  6. Bagatini IL, Eiler A, Bertilsson S, Klaveness D, Tessarolli LP, Vieira AAH (2014) Host-specificity and dynamics in bacterial communities associated with bloom-forming freshwater phytoplankton. PLoS One 9:e85950 https://doi.org/10.1371/journal.pone.0085950
  7. Bates SS, Gaudet J, Kaxzmarska I, Ehrman JM (2004) Interaction between bacteria and the domoic-acid-producing diatom Pseudo-nitzschia multiseries (Hasle) Hasle; can bacteria produce domoic acid autonomously? Harmful Algae 3:11-20 https://doi.org/10.1016/j.hal.2003.08.001
  8. Baty AE, Eastburn CC, Techkarnjanaruk S, Goodman AE, Geesey GG (2000) Spatial and temporal variations in chitinolytic gene expression and bacterial biomass production during chitin degradation. Appl Environ Microb 66:3574-3585 https://doi.org/10.1128/AEM.66.8.3574-3585.2000
  9. Behrenfeld MJ, Boss E, Siegel DA, Shea DM (2005) Carbon-based ocean productivity and phytoplankton physiology from space. Global Biogeochem Cy 19:GB1006. doi:10.1029/2004GB002299
  10. Bolch CJ, Bejoy TA, Green DH (2017) Bacterial associates modify growth dynamics of the dinoflagellate Gymnodinium catenatum. Front Microbiol 8:670. doi:10.3389/fmicb.2017.00670
  11. Buchan A, LeCleir GR, Gulvik CA, Gonzalez JM (2014) Master recycler: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol 12:686-698 https://doi.org/10.1038/nrmicro3326
  12. Carvalho RN, Bopp SK, Lettieri T (2011) Transcriptomics responses in marine diatom Thalassiosira pseudonana exposed to the polycyclic aromatic hydrocarbon benzo[a] pyrene. PLoS One 6:e26985 https://doi.org/10.1371/journal.pone.0026985
  13. Clarke KR, Warwick RM (2001) Change in marine communities : an approach to statistical analysis and interpretation. Plymouth Marine Laboratory, Plymouth, 176 p
  14. Crump BC, Armbrust EV, Baross JA (1999) Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia River, its estuary, and the adjacent coastal ocean. Appl Environ Microb 65:3192-3204
  15. Cruz-Lopez R, Maske H (2016) The vitamin $B_{1}$ and $B_{12}$ required by the marine dinoflagellate Lingulodinium polyedrum can be provided by its associated bacterial community in culture. Front Microbiol 7:1-13
  16. DeLong EF, Franks DG, Alldredge AL (1993) Phylogenetic diversity of aggregate-attached vs free-living marine bacterial assemblages. Limnol Oceanogr 38:924-934 https://doi.org/10.4319/lo.1993.38.5.0924
  17. Fernandez E, Serret P, Demadariaga I, Harbour DS, Davies AG (1992) Photosynthetic carbon metabolism and biochemical composition of spring phytoplankton assemblages enclosed in microcosms: the diatom-Phaeocystis sp. succession. Mar Ecol-Prog Ser 90:89-102 https://doi.org/10.3354/meps090089
  18. Finlay BJ, Monaghan EB, Maberly SC (2002) Hypothesis: the rate and scale of dispersal of freshwater diatom species is a function of their global abundance. Protist 153:261-273 https://doi.org/10.1078/1434-4610-00103
  19. Grossart HP, Levold F, Allgaier M, Simon M, Brinkhoff T (2005) Marine diatom species harbour distinct bacterial communities. Environ Microbiol 7:860-873 https://doi.org/10.1111/j.1462-2920.2005.00759.x
  20. Jasti S, Sieracki ME, Poulton NJ, Giewat MW, Rooney-Varga JN (2005) Phylogenetic diversity and specificity of bacteria closely associated with Alexandrium spp. and Other Phytoplankton. Appl Environ Microb 71:3483-3494 https://doi.org/10.1128/AEM.71.7.3483-3494.2005
  21. Kiorboe T, Ploug H, Thygesen UH (2001) Fluid motion and solute distribution around sinking aggregates. 1. Smallscale fluxes and heterogeneity of nutrients in the pelagic environment. Mar Ecol-Prog Ser 211:1-13 https://doi.org/10.3354/meps211001
  22. Lane DJ (1991) 16S/23S rRNA sequencing. In: E Stackebrandt, M Goodfellow (eds) Nucleic acid techniques in bacterial systematics. Chichester, United Kingdom, pp 115-175
  23. Li W, Fu L, Niu B, Wu S, Wooley J (2012) Ultrafast clustering algorithms for metagenomic sequence analysis. Brief Bioinform 13:656-668 https://doi.org/10.1093/bib/bbs035
  24. Mayali X, Azam F (2004) Algicidal bacteria in the sea and their impact on algal blooms. J Eukaryot Microbiol 51:139-144 https://doi.org/10.1111/j.1550-7408.2004.tb00538.x
  25. Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reactionamplified genes coding for 16S rRNA. Appl Environ Microb 59(3):695-700
  26. Park BS, Joo JH, Baek KD, Han MS (2016) A mutualistic interaction between the bacterium Pseudomonas asplenii and the harmful algal species Chattonella marina (Raphidophyceae). Harmful Algae 56:29-36 https://doi.org/10.1016/j.hal.2016.04.006
  27. Park BS, Wang P, Kim JH, Kim JH, Gobler CJ, Han MS (2014) Resolving the intra-specific succession within Cochlodinium polykrikoides populations in southern Korean coastal waters via use of quantitative PCR assays. Harmful Aglae 37:133-141 https://doi.org/10.1016/j.hal.2014.04.019
  28. Park BS, Guo R, Lim W-A, Ki J-S (2017) Importance of free-living and particle-associated bacteria for the growth of the harmful dinoflagellate Prorocentrum minimum: evidence in culture stages. Mar Freshwater Res. doi:10.1071/MF17102_AC (in press)
  29. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590-D596 https://doi.org/10.1093/nar/gks1219
  30. Reitan KI, Rainuzzo JR, Olsen Y (1994) Effect of nutrient limitation on fatty acid and lipid content of marine microalgae. J Phycol 30:972-979 https://doi.org/10.1111/j.0022-3646.1994.00972.x
  31. Rooney-Varga JN, Giewat MW, Savin MC, LeGresley M, Martin JL (2005) Links between phytoplankton and bacterial community dynamics in a coastal marine environment. Microb Ecol 49:163-175 https://doi.org/10.1007/s00248-003-1057-0
  32. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: opensource, platformindependent, community-supported software for describing and comparingmicrobial communities. Appl Environ Microb 75:7537-7541 https://doi.org/10.1128/AEM.01541-09
  33. Seyedsayamdost MR, Case RJ, Kolter R, Clardy J (2011) The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat Chem 3:331-335 https://doi.org/10.1038/nchem.1002
  34. Simon M, Glockner FO, Amann R (1999) Different community structure and temperature optima of heterotrophic picoplankton in various regions of the Southern Ocean. Aquat Microb Ecol 18:275-284 https://doi.org/10.3354/ame018275
  35. Sternberg C, Christensen BB, Johansen T, Nielsen AT, Andersen JB, Givskov M, Molin S (1999) Distribution of bacterial growth activity in flow-chamber biofilms. Appl Environ Microb 65:4108-4117
  36. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725-2729 https://doi.org/10.1093/molbev/mst197
  37. Taylor JD, Cottingham SD, Billinge J, Cunliffe M (2014) Seasonal microbial community dynamics correlate with phytoplankton-derived polysaccharides in surface coastal waters. ISME J 8:245-248 https://doi.org/10.1038/ismej.2013.178
  38. Thompson JD, Higgins DG, Gibbson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4690 https://doi.org/10.1093/nar/22.22.4673
  39. van Rijssel M, Janse I, Noordkamp DJB, Gieskes WWC (2000) An inventory of factors that affect polysaccharide production by Phaeocystis globose. J Sea Res 43:297-306 https://doi.org/10.1016/S1385-1101(00)00013-7
  40. Worm J, Sondergaard M (1998) Dynamics of heterotrophic bacteria attached to Microcystis spp. (Cyanobacteria). Aquat Microb Ecol 14:19-28 https://doi.org/10.3354/ame014019