Prokaryotic and eukaryotic microbiomes associated with blooms of the ichthyotoxic dinoflagellate Cochlodinium (Margalefidinium) polykrikoides in New York, USA, estuaries

English version

Autoři: Theresa K. Hattenrath-Lehmann ^aff001; Jennifer Jankowiak ^aff001; Florian Koch ^aff001; Christopher J. Gobler ^aff001
Působiště autorů: Stony Brook University, School of Marine and Atmospheric Sciences, Southampton, NY, United States of America ^aff001
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223067

Souhrn

While harmful algal blooms caused by the ichthyotoxic dinoflagellate, Cochlodinium (Margalefidinium) polykrikoides, are allelopathic and may have unique associations with bacteria, a comprehensive assessment of the planktonic communities associated with these blooms has been lacking. Here, we used high-throughput amplicon sequencing to assess size fractionated (0.2 and 5 μm) bacterial (16S) and phytoplankton assemblages (18S) associated with blooms of C. polykrikoides during recurrent blooms in NY, USA. Over a three-year period, samples were collected inside (‘patch’) and outside (‘non-patch’) dense accumulations of C. polykrikoides to assess the microbiome associated with these blooms. Eukaryotic plankton communities of blooms had significantly lower diversity than non-bloom samples, and non-bloom samples hosted 30 eukaryotic operational taxonomic units (OTUs) not found within blooms, suggesting they may have been allelopathically excluded from blooms. Differential abundance analyses revealed that C. polykrikoides blooms were significantly enriched in dinoflagellates (p<0.001) and the experimental enrichment of C. polykrikoides led to a significant increase in the relative abundance of eight genera of dinoflagellates but a significant decline in other eukaryotic plankton. Amoebophrya co-dominated both within- and near- C. polykrikoides blooms and was more abundant in bloom patches. The core bacterial microbiome of the >0.2μm fraction of blooms was dominated by an uncultured bacterium from the SAR11 clade, while the >5μm size fraction was co-dominated by an uncultured bacterium from Rhodobacteraceae and Coraliomargarita. Two bacterial lineages within the >0.2μm fraction, as well as the Gammaproteobacterium, Halioglobus, from the >5μm fraction were unique to the microbiome of blooms, while there were 154 bacterial OTUs only found in non-bloom waters. Collectively, these findings reveal the unique composition and potential function of eukaryotic and prokaryotic communities associated with C. polykrikoides blooms.

Klíčová slova:

Eukaryota – Bacteria – Algae – Microbiome – Microbial taxonomy – Dinoflagellates – Marine bacteria – Synechococcus

Zdroje

1. Margalef R (1961) Hidrografia y fitoplancton de un area marina de la costa meridional de Puerto Rico. Investigacio´n Pesquera 18: 76–78.

2. Kudela RM, Gobler CJ (2012) Harmful dinoflagellate blooms caused by Cochlodinium sp.: Global expansion and ecological strategies facilitating bloom formation. Harmful Algae 14: 71–86.

3. Tomas CR, Smayda TJ (2008) Red tide blooms of Cochlodinium polykrikoides in a coastal cove. Harmful Algae 7: 308–317.

4. Mulholland MR, Morse RE, Boneillo GE, Bernhardt PW, Filippino KC, Procise LA, et al. (2009) Understanding the causes and impacts of Cochlodinium polykrikoides blooms in the Chesapeake Bay. Estuaries & Coasts 32: 734–.

5. Marshall HG, Egerton TA, Burchardt L, Cerbin S, Kokocinski M (2005) Long term monitoring results of harmful algal populations in Chesapeake Bay and its major tributaries in Virginia, U.S.A. Ocean Hydrobiol Stud 34: 35–41.

6. Verity PG (2010) Expansion of potentially harmful algal taxa in a Georgia Estuary (USA). Harmful Algae 9: 144–152.

7. Phlips EJ, Badylak S, Christman M, Wolny J, Brame J, Garland J, et al. (2011) Scales of temporal and spatial variability in the distribution of harmful algae species in the Indian River Lagoon, Florida, USA. Harmful Algae 10: 277–290.

8. Gobler CJ, Burson A, Koch F, Tang YZ, Mulholland MR (2012) The role of nitrogenous nutrients in the occurrence of harmful algal blooms caused by Cochlodinium polykrikoides in New York estuaries (USA). Harmful Algae 17: 64–74.

9. Koch F, Burson A, Tang YZ, Collier JL, Fisher NS, Sañudo-Wilhelmy S, et al. (2014) Alteration of plankton communities and biogeochemical cycles by harmful Cochlodinium polykrikoides (Dinophyceae) blooms. Harmful Algae 33: 41–54.

10. Gobler CJ, Berry DL, Anderson OR, Burson A, Koch F, Rodgers BS, et al. (2008) Characterization, dynamics, and ecological impacts of harmful Cochlodinium polykrikoides blooms on eastern Long Island, NY, USA. Harmful Algae 7: 293–307.

11. Nuzzi R (2004) Cochlodinium polykrikoides in the Peconic Estuary. In: Wyatt T, editor. Harmful Algae News. Paris: UNESCO. pp. 10–11.

12. Rheuban JE, Williamson S, Costa JE, Glover DM, Jakuba RW, McCorkle DC, et al. (2016) Spatial and temporal trends in summertime climate and water quality indicators in the coastal embayments of Buzzards Bay, Massachusetts. Biogeosciences 13: 253–265.

13. Richlen ML, Morton SL, Jamali EA, Rajan A, Anderson DM (2010) The catastrophic 2008–2009 red tide in the Arabian gulf region, with observations on the identification and phylogeny of the fish-killing dinoflagellate Cochlodinium polykrikoides. Harmful Algae 9: 163–172.

14. Matsuoka K, Iwataki M, Kawami H (2008) Morphology and taxonomy of chain-forming species of the genus Cochlodinium (Dinophyceae). Harmful Algae 7: 261–270.

15. Whyte JNC, Haigh N, Ginther NG, Keddy LJ (2001) First record of blooms of Cochlodinium sp. (Gymnodiniales, Dinophyceae) causing mortality to aquacultured salmon on the west coast of Canada. Phycologia 40: 298–304.

16. Kim CS, Lee SG, Lee CK, Kim HG, Jung J (1999) Reactive oxygen species as causative agents in the ichthyotoxicity of the red tide dinoflagellate Cochlodinium polykrikoides. Journal of Plankton Research 21: 2105–2115.

17. Kim HG (1998) Harmful algal blooms in Korean coastal waters focused on three fish killing dinoflagellates. In: Lee H, Lee S, Lee C, editors. Harmful Algal Blooms in Korea and China. Pusan, Korea: NFRDI.

18. Tang YZ, Koch F, Gobler CJ (2010) Most harmful algal bloom species are vitamin B1 and B12 auxotrophs. Proceedings of the National Academy of Sciences 107: 20756–20761.

19. Jeong HJ, Yoo YD, Kim JS, Kim TH, Kim JH, Kang NS, et al. (2004) Mixotrophy in the Phototrophic Harmful Alga Cochlodinium polykrikoides (Dinophycean): Prey Species, the Effects of Prey Concentration, and Grazing Impact. Journal of Eukaryotic Microbiology 51: 563–569. doi: 10.1111/j.1550-7408.2004.tb00292.x 15537091

20. Jeong HJ, Yoo YD, Kim JS, Seong KA, Kang NS, Kim TH (2010) Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Science Journal 45: 65–91.

21. Jiang XD, Lonsdale DJ, Gobler CJ (2010) Density-dependent nutritional value of the dinoflagellate Cochlodinium polykrikoides to the copepod Acartia tonsa. Limnology and Oceanography 55: 1643–1652.

22. Jiang XD, Lonsdale DJ, Gobler CJ (2010) Grazers and vitamins shape chain formation in a bloom-forming dinoflagellate, Cochlodinium polykrikoides Oecologia 164: 1133–1133.

23. Tang YZ, Gobler CJ (2010) Allelopathic effects of Cochlodinium polykrikoides isolates and blooms from the estuaries of Long Island, New York, on co-occurring phytoplankton. Marine Ecology Progress Series 406: 19–31.

24. Tang YZ, Gobler CJ (2012) The toxic dinoflagellate Cochlodinium polykrikoides (Dinophyceae) produces resting cysts. Harmful Algae 20: 71–80.

25. Hattenrath-Lehmann TK, Zhen Y, Wallace RB, Tang Y-Z, Gobler CJ (2016) Mapping the distribution of cysts from the toxic dinoflagellate Cochlodinium polykrikoides in bloom-prone estuaries by a novel fluorescence in situ hybridization assay. Applied and Environmental Microbiology 82: 1114–1125. doi: 10.1128/AEM.03457-15 26637596

26. Li Z, Han M-S, Matsuoka K, Kim S-Y, Shin HH (2015) Identification of the resting cyst of Cochlodinium polykrikoides Margalef (Dinophyceae, Gymnodiniales) in Korean coastal sediments. Journal of Phycology 51: 204–210. doi: 10.1111/jpy.12252 26986269

27. Jung SW, Kang D, Kim H-J, Shin HH, Park JS, Park SY, et al. (2018) Mapping distribution of cysts of recent dinoflagellate and Cochlodinium polykrikoides using next-generation sequencing and morphological approaches in South Sea, Korea. Scientific Reports 8: 7011. doi: 10.1038/s41598-018-25345-4 29725114

28. Griffith AW, Doherty OM, Gobler CJ (2019) Ocean warming along temperate western boundaries of the Northern Hemisphere promotes an expansion of Cochlodinium polykrikoides blooms. Proc Biol Sci 286: 20190340. doi: 10.1098/rspb.2019.0340 31161913

29. Oh J-I, Kim M-J, Lee J-Y, Ko I-J, Kim W, Kim SW (2011) Isolation and characterization of algicidal bacteria from Cochlodinium polykrikoides culture. Biotechnology and Bioprocess Engineering 16: 1124–1133.

30. Kim M-J, Jeong S-Y, Lee S-J (2008) Isolation, identification, and algicidal activity of marine bacteria against Cochlodinium polykrikoides. Journal of Applied Phycology 20: 1069–1078.

31. Lee BK, Katano T, Kitamura S, Oh MJ, Han MS (2008) Monitoring of algicidal bacterium, Alteromonas sp. strain A14 in its application to natural Cochlodinium polykrikoides blooming seawater using fluorescence in situ hybridization. J Microbiol 46: 274–282. doi: 10.1007/s12275-007-0238-9 18604496

32. Park BS, Kim J-H, Kim JH, Gobler CJ, Baek SH, Han M-S (2015) Dynamics of bacterial community structure during blooms of Cochlodinium polykrikoides (Gymnodiniales, Dinophyceae) in Korean coastal waters. Harmful Algae 48: 44–54. doi: 10.1016/j.hal.2015.07.004 29724475

33. Xiao X, Sogge H, Lagesen K, Tooming-Klunderud A, Jakobsen KS, Rohrlack T (2014) Use of high throughput sequencing and light microscopy show contrasting results in a study of phytoplankton occurrence in a freshwater environment. PLoS ONE 9: e106510. doi: 10.1371/journal.pone.0106510 25171164

34. Lindeque PK, Parry HE, Harmer RA, Somerfield PJ, Atkinson A (2013) Next Generation Sequencing Reveals the Hidden Diversity of Zooplankton Assemblages. PLOS ONE 8: e81327. doi: 10.1371/journal.pone.0081327 24244737

35. Stern R, Kraberg A, Bresnan E, Kooistra WHCF, Lovejoy C, Montresor M, et al. (2018) Molecular analyses of protists in long-term observation programmes—current status and future perspectives. Journal of Plankton Research 40: 519–536.

36. Yang C, Li Y, Zhou B, Zhou Y, Zheng W, Tian Y, et al. (2015) Illumina sequencing-based analysis of free-living bacterial community dynamics during an Akashiwo sanguine bloom in Xiamen sea, China. Scientific Reports 5: 8476. doi: 10.1038/srep08476 25684124

37. Li J, Zhang J, Liu L, Fan Y, Li L, Yang Y, et al. (2015) Annual periodicity in planktonic bacterial and archaeal community composition of eutrophic Lake Taihu. Scientific Reports 5: 15488. doi: 10.1038/srep15488 26503553

38. Sison-Mangus MP, Jiang S, Tran KN, Kudela RM (2014) Host-specific adaptation governs the interaction of the marine diatom, Pseudo-nitzschia and their microbiota. The ISME Journal 8: 63–76. doi: 10.1038/ismej.2013.138 23985747

39. Hattenrath-Lehmann TK, Gobler CJ (2017) Identification of unique microbiomes associated with harmful algal blooms caused by Alexandrium fundyense and Dinophysis acuminata. Harmful Algae 68: 17–30. doi: 10.1016/j.hal.2017.07.003 28962978

40. Park BS, Guo R, Lim W-A, Ki JS (2017) Pyrosequencing reveals specific associations of bacterial clades Roseobacter and Flavobacterium with the harmful dinoflagellate Cochlodinium polykrikoides growing in culture. Marine Ecology 38: e12474.

41. Shin H, Lee E, Shin J, Ko SR, Oh HS, Ahn CY (2018) Elucidation of the bacterial communities associated with the harmful microalgae Alexandrium tamarense and Cochlodinium polykrikoides using nanopore sequencing. 8: 5323. doi: 10.1038/s41598-018-23634-6 29593350

42. de Vargas C, Audic S, Henry N, Decelle J, Mahé F, Logares R, et al. (2015) Eukaryotic plankton diversity in the sunlit ocean. Science 348.

43. Dempster EL, Pryor KV, Francis D, Young JE, Rogers HJ (1999) Rapid DNA extraction from ferns for PCR-based analyses. Biotechniques 27: 66–68. doi: 10.2144/99271bm13 10407666

44. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, et al. (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research 41: e1–e1. doi: 10.1093/nar/gks808 22933715

45. Hadziavdic K, Lekang K, Lanzen A, Jonassen I, Thompson EM, Troedsson C (2014) Characterization of the 18S rRNA gene for designing universal eukaryote specific primers. PLoS ONE 9: e87624. doi: 10.1371/journal.pone.0087624 24516555

46. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nature methods 7: 335–336. doi: 10.1038/nmeth.f.303 20383131

47. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460–2461. doi: 10.1093/bioinformatics/btq461 20709691

48. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26: 266–267. doi: 10.1093/bioinformatics/btp636 19914921

49. Jankowiak J, Hattenrath-Lehmann T, Kramer BJ, Ladds M, Gobler CJ (2019) Deciphering the effects of nitrogen, phosphorus, and temperature on cyanobacterial bloom intensification, diversity, and toxicity in western Lake Erie. Limnology and Oceanography.

50. Huang S, Wilhelm SW, Harvey HR, Taylor K, Jiao N, Chen F (2012) Novel lineages of Prochlorococcus and Synechococcus in the global oceans. The ISME journal 6: 285–297. doi: 10.1038/ismej.2011.106 21955990

51. Doblin MA, Blackburn SI, Hallegraeff GM (1999) Growth and biomass stimulation of the toxic dinoflagellate Gymnodinium catenatum (Graham) by dissolved organic substances. Journal of Experimental Marine Biology and Ecology 236: 33–47.

52. Gobler CJ, Deonarine S, Leigh-Bell J, Gastrich MD, Anderson OR, Wilhelm SW (2004) Ecology of phytoplankton communities dominated by Aureococcus anophagefferens: the role of viruses, nutrients, and microzooplankton grazing. Harmful Algae 3: 471–483.

53. Oliveros JC (2007–2015) Venny. An interactive tool for comparing lists with Venn's diagrams. http://bioinfogp.cnb.csic.es/tools/venny/index.html.

54. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biology 11: R106. doi: 10.1186/gb-2010-11-10-r106 20979621

55. McMurdie PJ, Holmes S (2013) phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLOS ONE 8: e61217. doi: 10.1371/journal.pone.0061217 23630581

56. McMurdie PJ, Holmes S (2015) Shiny-phyloseq: Web application for interactive microbiome analysis with provenance tracking. Bioinformatics 31: 282–283. doi: 10.1093/bioinformatics/btu616 25262154

57. Borcard D, Gillet F, Legendre P (2018) Numerical ecology with R.: Springer.

58. Ye Y, Doak TG (2009) A Parsimony Approach to Biological Pathway Reconstruction/Inference for Genomes and Metagenomes. PLOS Computational Biology 5: e1000465. doi: 10.1371/journal.pcbi.1000465 19680427

59. Louca S, Doebeli M (2018) Efficient comparative phylogenetics on large trees. Bioinformatics 34: 1053–1055. doi: 10.1093/bioinformatics/btx701 29091997

60. Barbera P, Kozlov AM, Czech L, Morel B, Darriba D, Flouri T, et al. (2019) EPA-ng: Massively Parallel Evolutionary Placement of Genetic Sequences. Syst Biol 68: 365–369. doi: 10.1093/sysbio/syy054 30165689

61. Douglas GM, Maffei VJ, Zaneveld J, Yurgel SN, Brown JR, Taylor CM, et al. (2019) PICRUSt2: An improved and extensible approach for metagenome inference. bioRxiv: 672295.

62. Czech L, Stamatakis A (2019) Scalable methods for analyzing and visualizing phylogenetic placement of metagenomic samples. PLOS ONE 14: e0217050. doi: 10.1371/journal.pone.0217050 31136592

63. Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics (Oxford, England) 30: 3123–3124.

64. 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.

65. Metfies K, Schroeder F, Hessel J, Wollschlager J, Micheller S, Wolf C, et al. (2016) High-resolution monitoring of marine protists based on an observation strategy integrating automated on-board filtration and molecular analyses. Ocean Science 12: 1237–1247.

66. Coats DW, Adam EJ, Gallegos CL, Hedrick S (1996) Parasitism of photosynthetic dinoflagellates in a shallow subestuary of Chesapeake Bay, USA. Aquatic Microbial Ecology 11: 1–9.

67. Coats DW, Park MG (2002) Parasitism of photosynthetic dinoflagellates by three strains of Amoebophrya (Dinophyta): Parasite survival, infectivity, generation time, and host specificity. Journal of Phycology 38: 520–528.

68. Park MG, Kim S, Shin E-Y, Yih W, Coats DW (2013) Parasitism of harmful dinoflagellates in Korean coastal waters. Harmful Algae 30, Supplement 1: S62–S74.

69. Thangaraj P, Park TG, Ki J-S (2017) Molecular cloning reveals co-occurring species behind red tide blooms of the harmful dinoflagellate Cochlodinium polykrikoides. Biochemical Systematics and Ecology 70: 29–34.

70. Kim S, Park MG (2014) Amoebophrya spp. from the bloom-forming dinoflagellate Cochlodinium polykrikoides: parasites not nested in the "Amoebophrya ceratii complex". J Eukaryot Microbiol 61: 173–181. doi: 10.1111/jeu.12097 24612333

71. Park BS, Kim S, Kim J-H, Ho Kim J, Han M-S (2019) Dynamics of Amoebophrya parasites during recurrent blooms of the ichthyotoxic dinoflagellate Cochlodinium polykrikoides in Korean coastal waters. Harmful Algae 84: 119–126. doi: 10.1016/j.hal.2019.02.001 31128796

72. Hattenrath-Lehmann TK, Gobler CJ (2011) Allelopathic inhibition of competing phytoplankton by North American strains of the toxic dinoflagellate, Alexandrium fundyense: Evidence from field experiments, laboratory experiments, and bloom events. Harmful Algae 11: 106–116.

73. Poulson KL, Sieg RD, Prince EK, Kubanek J (2010) Allelopathic compounds of a red tide dinoflagellate have species-specific and context-dependent impacts on phytoplankton. Marine Ecology Progress Series 416: 69–78.

74. Prince EK, Myers TL, Naar J, Kubanek J (2008) Competing phytoplankton undermines allelopathy of a bloom-forming dinoflagellate. Proceedings of the Royal Society B-Biological Sciences 275: 2733–2741.

75. Fistarol GO, Legrand C, Graneli E (2003) Allelopathic effect of Prymnesium parvum on a natural plankton community. Marine Ecology Progress Series 255: 115–125.

76. Weissbach A, Tillmann U, Legrand C (2010) Allelopathic potential of the dinoflagellate Alexandrium tamarense on marine microbial communities. Harmful Algae 10: 9–18.

77. Buchan A, LeCleir GR, Gulvik CA, Gonzalez JM (2014) Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Micro 12: 686–698.

78. Wichels A, Hummert C, Elbrächter M, Luckas B, Schütt C, Gerdts G (2004) Bacterial diversity in toxic Alexandrium tamarense blooms off the Orkney Isles and the Firth of Forth. Helgoland Marine Research 58: 93–103.

79. 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. Applied and Environmental Microbiology 71: 3483–3494. doi: 10.1128/AEM.71.7.3483-3494.2005 16000752

80. Guannel ML, Horner-Devine MC, Rocap G (2011) Bacterial community composition differs with species and toxigenicity of the diatom Pseudo-nitzschia. Aquatic Microbial Ecology 64: 117–133.

81. Garces E, Vila M, Rene A, Alonso-Saez L, Angles S, Luglie A, et al. (2007) Natural bacterioplankton assemblage composition during blooms of Alexandrium spp. (Dinophyceae) in NW Mediterranean coastal waters. Aquatic Microbial Ecology 46: 55–70.

82. Hasegawa Y, Martin JL, Giewat MW, Rooney-Varga JN (2007) Microbial community diversity in the phycosphere of natural populations of the toxic alga, Alexandrium fundyense. Environmental Microbiology 9: 3108–3121. doi: 10.1111/j.1462-2920.2007.01421.x 17991038

83. Zhou J, Richlen ML, Sehein TR, Kulis DM, Anderson DM, Cai Z (2018) Microbial community structure and associations during a marine dinoflagellate bloom. Frontiers in Microbiology 9.

84. Kirchman DL (2016) Growth rates of microbes in the oceans. Annual Review of Marine Science 8: 285–309. doi: 10.1146/annurev-marine-122414-033938 26195108

85. Tang YZ, Gobler CJ (2009) Characterization of the toxicity of Csochlodinium polykrikoides isolates from Northeast US estuaries to finfish and shellfish. Harmful Algae 8: 454–462.

86. Landa M, Blain S, Christaki U, Monchy S, Obernosterer I (2016) Shifts in bacterial community composition associated with increased carbon cycling in a mosaic of phytoplankton blooms. The ISME journal 10: 39–50. doi: 10.1038/ismej.2015.105 26196334

87. Zhao Y, Wang ZB, Xu JX (2003) Effect of cytochrome c on the generation and elimination of O2*- and H2O2 in mitochondria. J Biol Chem 278: 2356–2360. doi: 10.1074/jbc.M209681200 12435729

88. Bowman SE, Bren KL (2008) The chemistry and biochemistry of heme c: functional bases for covalent attachment. Nat Prod Rep 25: 1118–1130. doi: 10.1039/b717196j 19030605

89. Herlemann DPR, Lundin D, Labrenz M, Jürgens K, Zheng Z, Aspeborg H, et al. (2013) Metagenomic de novo assembly of an aquatic representative of the verrucomicrobial class Spartobacteria. mBio 4: e00569.

90. Lee JS (1996) Bioactive components from the red tide plankton Cochlodinium polykrikoides. J Korean Fish Soc 29: 165–173.

91. Elifantz H, Malmstrom RR, Cottrell MT, Kirchman DL (2005) Assimilation of Polysaccharides and Glucose by Major Bacterial Groups in the Delaware Estuary. Applied and Environmental Microbiology 71: 7799. doi: 10.1128/AEM.71.12.7799-7805.2005 16332754

92. Jousset A, Bienhold C, Chatzinotas A, Gallien L, Gobet A, Kurm V, et al. (2017) Where less may be more: how the rare biosphere pulls ecosystems strings. Isme j 11: 853–862. doi: 10.1038/ismej.2016.174 28072420

93. Koch F, Hattenrath-Lehmann TK, Goleski JA, Sanudo-Wilhelmy S, Fisher NS, Gobler CJ (2012) Vitamin B1 and B12 uptake and cycling by plankton communities in coastal ecosystems. Frontiers in Microbiology 3.

94. Sañudo-Wilhelmy SA, Cutter LS, Durazo R, Smail EA, Gómez-Consarnau L, Webb EA, et al. (2012) Multiple B-vitamin depletion in large areas of the coastal ocean. Proceedings of the National Academy of Sciences 109: 14041–14045.

95. Heal KR, Qin W, Ribalet F, Bertagnolli AD, Coyote-Maestas W, Hmelo LR, et al. (2017) Two distinct pools of B12 analogs reveal community interdependencies in the ocean. Proceedings of the National Academy of Sciences 114: 364–369.

96. Jeong HJ, Park JY, Nho JH, Park MO, Ha JH, Seong KA, et al. (2005) Feeding by red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquatic Microbial Ecology 41: 131–143.

97. Seong KA, Jeong HJ, Kim S, Kim GH, Kang JH (2006) Bacterivory by co-occurring red-tide algae, heterotrophic nanoflagellates, and ciliates. Marine Ecology Progress Series 322: 85–97.

Prokaryotic and eukaryotic microbiomes associated with blooms of the ichthyotoxic dinoflagellate Cochlodinium (Margalefidinium) polykrikoides in New York, USA, estuaries

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz