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Effects of Hypoxia on the Phylogenetic Composition and Species Distribution of Protists in a Subtropical Harbor

  • Environmental Microbiology
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Abstract

Tolo Harbor, a subtropical semi-enclosed coastal water body, is surrounded by an expanding urban community, which contributes to large concentrations of nutrient runoff, leading to algal blooms and localized hypoxic episodes. Present knowledge of protist distributions in subtropical waters during hypoxic conditions is very limited. In this study, therefore, we combined parallel 454 pyrosequencing technology and denaturing gradient gel electrophoresis (DGGE) fingerprint analyses to reveal the protist community shifts before, during, and after a 2-week hypoxic episode during the summer of 2011. Hierarchical clustering for DGGE demonstrated similar grouping of hypoxic samples separately from oxic samples. Dissolved oxygen (DO) concentration and dissolved inorganic nitrogen:phosphate (DIN:PO4) concentrations significantly affected OTU distribution in 454 sequenced samples, and a shift toward a ciliate and marine alveolate clade II (MALV II) species composition occurred as waters shifted from oxic to hypoxic. These results suggest that protist community shifts toward heterotrophic and parasitic tendencies as well as decreased diversity and richness in response to hypoxic outbreaks.

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References

  1. Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929. doi:10.1126/science.1156401

    Article  CAS  PubMed  Google Scholar 

  2. Edgcomb V, Orsi W, Bunge J, Jeon S, Christen R, Leslin C, Holder M, Taylor GT, Suarez P, Varela R, Epstein S (2011) Protistan microbial observatory in the Cariaco Basin, Caribbean. I. Pyrosequencing vs Sanger insights into species richness. ISME J 5:1344–1356. doi:10.1038/ismej.2011.6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. López-García P, Rodríguez-Valera F, Pedrós-Alió C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–607. doi:10.1038/35054537

    Article  PubMed  Google Scholar 

  4. Moon-van der Staay SY, De Wachter R, Vaulot D (2001) Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409:607–610. doi:10.1038/35054541

    Article  CAS  PubMed  Google Scholar 

  5. Diez B, Pedros-alio C, Massana R, Pedro C, Di B (2001) Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl Environ Microbiol 67:2932–2941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Worden AZ, Nolan JK, Palenik B (2004) Assessing the dynamics and ecology of marine picophytoplankton: the importance of the eukaryotic component. Limnol Oceanogr 49:168–179

    Article  CAS  Google Scholar 

  7. Cheung MK, Au CH, Chu KH, Kwan HS, Wong CK (2010) Composition and genetic diversity of picoeukaryotes in subtropical coastal waters as revealed by 454 pyrosequencing. ISME J 4:1053–1059. doi:10.1038/ismej.2010.26

    Article  PubMed  Google Scholar 

  8. Cheung MK, Chu KH, Li CP, Kwan HS, Wong CK (2008) Genetic diversity of picoeukaryotes in a semi-enclosed harbour in the subtropical western Pacific Ocean. Aquat Microb Ecol 53:295–305. doi:10.3354/ame01247

    Article  Google Scholar 

  9. Jing H, Liu H, Bird DF, Wong THC, Chen X, Chen B (2010) Composition and seasonal variability of picoeukaryote communities at two subtropical coastal sites with contrasting trophic conditions. J Plankton Res 32:565–573. doi:10.1093/plankt/fbq002

    Article  CAS  Google Scholar 

  10. Groisillier A, Massana R, Valentin K, Vaulot D, Guillou L (2006) Genetic diversity and habitats of two enigmatic marine alveolate lineages. Aquat Microb Ecol 42:277–291. doi:10.3354/ame042277

    Article  Google Scholar 

  11. Orsi W, Song YC, Hallam S, Edgcomb V (2012) Effect of oxygen minimum zone formation on communities of marine protists. ISME J 6:1586–1601. doi:10.1038/ismej.2012.7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Wu RSS (2002) Hypoxia: from molecular responses to ecosystem responses. Mar Pollut Bull 45:35–45

    Article  CAS  PubMed  Google Scholar 

  13. Zhang J, Gilbert D, Gooday AJ, Levin L, Naqvi SW, Middelburg JJ, Scranton M, Ekau W, Peña A, Dewitte B, Oguz T, Monteiro PMS, Urban E, Rabalais NN, Ittekkot V, Kemp WM, Ulloa O, Elmgren R, Escobar-Briones E, Van der Plas AK (2010) Natural and human-induced hypoxia and consequences for coastal areas: synthesis and future development. Biogeosciences 7:1443–1467. doi:10.5194/bg-7-1443-2010

    Article  CAS  Google Scholar 

  14. Guillou L, Viprey M, Chambouvet A, Welsh RM, Kirkham AR, Massana R, Scanlan DJ, Worden AZ (2008) Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environ Microbiol 10:3349–3365. doi:10.1111/j.1462-2920.2008.01731.x

    Article  CAS  PubMed  Google Scholar 

  15. Rocke E, Jing H, Liu H (2012) Phylogenetic composition and distribution of picoeukaryotes in the hypoxic northwestern coast of the Gulf of Mexico. Microbiologyopen 2:130–143. doi:10.1002/mbo3.57

    Article  PubMed  PubMed Central  Google Scholar 

  16. Xu J, Yin K, Liu H, Lee JHW, Anderson DM, Ho AYT, Harrison PJ (2010) A comparison of eutrophication impacts in two harbours in Hong Kong with different hydrodynamics. J Mar Syst 83:276–286. doi:10.1016/j.jmarsys.2010.04.002

    Article  Google Scholar 

  17. Knap A, Michael, A., Close, A. et al. (eds) (1996) Protocols for the Joint Global Ocean Flux Study (JGOFS) core measurements. GOFS Report Nr 19, Viþ170 pp (reprint of the IOC Manuals and Guides No 29, UNESCO 1994): 43–110

  18. Marie D, Partensky F, Jacquet S, Vaulot D (1997) 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

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Bostrom KH, Simu K, Hagstrom A, Riemann L (2004) Optimization of DNA extraction for quantitative marine bacterioplankton community analysis. Limnol Oceanogr-Methods 2:365–373

    Article  Google Scholar 

  20. Casamayor EO, Massana R, Benlloch S, Ovreas L, Diez B, Goddard VJ, Gasol JM, Joint I, Rodriguez-Valera F, Pedros-Alio C (2002) Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern. Environ Microbiol 4:338–348. doi:10.1046/j.1462-2920.2002.00297.x

    Article  PubMed  Google Scholar 

  21. Lepere C, Boucher D, Jardillier L, Domaizon I, Debroas D (2006) Succession and regulation factors of small eukaryote community composition in a lacustrine ecosystem (Lake Pavin). Appl Environ Microbiol 72:2971–2981. doi:10.1128/AEM.72.4.2971-2981.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Daigle D, Simen BB, Pochart P (2011) High-throughput sequencing of PCR products tagged with universal primers using 454 life sciences systems. Curr Protoc Mol Biol Chapter 7: Unit7 5. doi: 10.1002/0471142727.mb0705s96

  23. Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ (2011) Removing noise from pyrosequenced amplicons. BMC Bioinforma 12:38. doi:10.1186/1471-2105-12-38

    Article  Google Scholar 

  24. 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: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi:10.1128/AEM.01541-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11:265–270

    Google Scholar 

  26. Lee SM, Chao A (1994) Estimating population size via sample coverage for closed capture-recapture models. Biometrics 50:88–97

    Article  CAS  PubMed  Google Scholar 

  27. Jari Oksanen FGB, Roeland Kindt, Pierre Legendre, Peter R. Minchin RBOH, Gavin L. Simpson, Peter Solymos, M., Wagner. HHSaH (2013) vegan: community ecology package. R package version 2.0-8

  28. Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, Boutte C, Burgaud G, de Vargas C, Decelle J, del Campo J, Dolan JR, Dunthorn M, Edvardsen B, Holzmann M, Kooistra WHCF, Lara E, Le Bescot N, Logares R, Mahé F, Massana R, Montresor M, Morard R, Not F, Pawlowski J, Probert I, Sauvadet A-L, Siano R, Stoeck T, Vaulot D, Zimmermann P, Christen R (2012) The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res 41:D597–D604. doi:10.1093/nar/gks1160

    Article  PubMed  PubMed Central  Google Scholar 

  29. 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. doi:10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Stoeck T, Behnke A, Christen R, Amaral-Zettler L, Rodriguez-Mora MJ, Chistoserdov A, Orsi W, Edgcomb VP (2009) Massively parallel tag sequencing reveals the complexity of anaerobic marine protistan communities. BMC Biol 7:72. doi:10.1186/1741-7007-7-72

    Article  PubMed  PubMed Central  Google Scholar 

  31. Massana R (2011) Eukaryotic picoplankton in surface oceans. Annu Rev Microbiol 65:91–110. doi:10.1146/annurev-micro-090110-102903

    Article  CAS  PubMed  Google Scholar 

  32. Edgcomb VP, Pachiadaki M (2014) Ciliates along oxyclines of permanently stratified marine water columns. J Eukaryot Microbiol 61:434–445. doi:10.1111/jeu.12122

    Article  CAS  PubMed  Google Scholar 

  33. Xu J, Yin KD, He L, Yuan XC, Ho AYT, Harrison PJ (2008) Phosphorus limitation in the northern South China Sea during late summer: influence of the Pearl River. Deep-Sea Res Part I-Oceanogr Res Papers 55:1330–1342. doi:10.1016/j.dsr.2008.05.007

    Article  CAS  Google Scholar 

  34. Countway PD, Vigil PD, Schnetzer A, Moorthi SD, Caron DA (2010) Seasonal analysis of protistan community structure and diversity at the USC Microbial Observatory (San Pedro Channel, North Pacific Ocean). Limnol Oceanogr 55:2381–2396

    Article  Google Scholar 

  35. Edgcomb VP, Bernhard JM (2013) Heterotrophic protists in hypersaline microbial mats and deep hypersaline basin water columns. Life (Basel) 3:346–362. doi:10.3390/life3020346

    CAS  PubMed Central  Google Scholar 

  36. Orsi W, Edgcomb V, Jeon S, Leslin C, Bunge J, Taylor GT, Varela R, Epstein S (2011) Protistan microbial observatory in the Cariaco Basin, Caribbean. II. Habitat specialization. ISME J 5:1357–1373. doi:10.1038/ismej.2011.7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Stock A, Jürgens K, Bunge J, Stoeck T (2009) Protistan diversity in suboxic and anoxic waters of the Gotland Deep (Baltic Sea) as revealed by 18S rRNA clone libraries. Aquat Microb Ecol 55:267–284. doi:10.3354/ame01301

    Article  Google Scholar 

  38. Yuan XY, Kedong, Harrison PJ, He L, Xu J (2011) Variations in apparent oxygen utilization and effects of P addition on bacterial respiration in subtropical Hong Kong waters. Estuar Coasts 34:536–543

    Article  CAS  Google Scholar 

  39. Lie AA, Wong CK, Lam JY, Liu JH, Yung YK (2011) Changes in the nutrient ratios and phytoplankton community after declines in nutrient concentrations in a semi-enclosed bay in Hong Kong. Mar Environ Res 71:178–188. doi:10.1016/j.marenvres.2011.01.001

    Article  CAS  PubMed  Google Scholar 

  40. Edgcomb VP, Kysela DT, Teske A, de Vera Gomez A, Sogin ML (2002) Benthic eukaryotic diversity in the Guaymas Basin hydrothermal vent environment. Proc Natl Acad Sci U S A 99:7658–7662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lopez-Garcia P, Herve P, Francoise G, Moreira D (2003) Autochthonous eukaryotic diversity in hydrothermal sediment and experimental microcolonizers at the Mid-Atlantic Ridge. Proc Natl Acad Sci U S A 100:697–702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Stoeck T, Hayward B, Taylor GT, Varela R, Epstein SS (2006) A multiple PCR-primer approach to access the microeukaryotic diversity in environmental samples. Protist 157:31–43. doi:10.1016/j.protis.2005.10.004

    Article  CAS  PubMed  Google Scholar 

  43. Takishita K, Yubuki N, Kakizoe N, Inagaki Y, Maruyama T (2007) Diversity of microbial eukaryotes in sediment at a deep-sea methane cold seep: surveys of ribosomal DNA libraries from raw sediment samples and two enrichment cultures. Extremophiles 11:563–576. doi:10.1007/s00792-007-0068-z

    Article  CAS  PubMed  Google Scholar 

  44. Massana R, Balague V, Guillou L, Pedros-Alio C (2004) Picoeukaryotic diversity in an oligotrophic coastal site studied by molecular and culturing approaches. FEMS Microbiol Ecol 50:231–243. doi:10.1016/j.femsec.2004.07.001

    Article  CAS  PubMed  Google Scholar 

  45. Not F, Gausling R, Azam F, Heidelberg JF, Worden AZ (2007) Vertical distribution of picoeukaryotic diversity in the Sargasso Sea. Environ Microbiol 9:1233–1252. doi:10.1111/j.1462-2920.2007.01247.x

    Article  CAS  PubMed  Google Scholar 

  46. Romari K, Daniel V (2004) Composition and temporal variability of picoeukaryote communities at a coastal site of the English Channel from 18S rDNA sequences. Limnol Oceanogr 49:784–798

    Article  Google Scholar 

  47. Worden A (2006) Picoeukaryote diversity in coastal waters of the Pacific Ocean. Aquat Microb Ecol 43:165–175. doi:10.3354/ame043165

    Article  Google Scholar 

  48. Chambouvet A, Morin P, Marie D, Guillou L (2008) Control of toxic marine dinoflagellate blooms by serial parasitic killers. Science (New York, NY) 322:1254–1257. doi:10.1126/science.116438

    Article  CAS  Google Scholar 

  49. Montagnes DJS, Chambouvet A, Guillou L, Fenton A (2008) Responsibility of microzooplankton and parasite pressure for the demise of toxic dinoflagellate blooms. Aquat Microb Ecol 53:211–225. doi:10.3354/ame01245

    Article  Google Scholar 

  50. Nielsen MV (1996) Growth and chemical composition of the toxic dinoflagellate Gymnodinium galatheanum in relation to irradiance, temperature and salinity. Mar Ecol-Prog Ser 136:205–211. doi:10.3354/meps136205

    Article  CAS  Google Scholar 

  51. Smayda TJ (1997) Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol Oceanogr 42:1137–1153

    Article  Google Scholar 

  52. Steidinger KA, Burkholder JM, Glasgow HB, Hobbs CW, Garrett JK, Truby EW, Noga EJ, Smith SA (1996) Pfiesteria piscicida gen. et sp. nov. (Pfiesteriaceae fam. nov.), a new toxic dinoflagellate with a complex life cycle and behavior. J Phycol 32:157–164. doi:10.1111/j.0022-3646.1996.00157.x

    Article  Google Scholar 

  53. Lin X, Scranton MI, Christoserdov AY, Varela R (2008) Spatiotemporal dynamics of bacterial populations in the anoxic Cariaco Basin. Limnol Oceanogr 53:37–51

    Article  CAS  Google Scholar 

  54. Bręk-Laitinen G, López Bellido J, Ojala A (2012) Response of a microbial food web to prolonged seasonal hypoxia in a boreal lake. Aquat Biol 14:105–120. doi:10.3354/ab00379

    Article  Google Scholar 

  55. Rocke E, Liu H (2014) Respiration, growth and grazing rates of three ciliate species in hypoxic conditions. Mar Pollut Bull 85:410–417. doi:10.1016/j.marpolbul.2014.04.050

    Article  CAS  PubMed  Google Scholar 

  56. Massana R, Guillou L, Díez B, Pedro C (2002) Unveiling the organisms behind novel eukaryotic ribosomal DNA sequences from the ocean. Appl Environ Microbiol 68:4554. doi:10.1128/AEM.68.9.4554-4558.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Schnepf E, Deichgra G, Hegewald E, Soeder CJ (1971) Electron microscopic observations on parasites of Scenedesmus mass cultures: 3. Chytridium sp. Arch Mikrobiol 75:230. doi:10.1007/bf00408984

    Article  Google Scholar 

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Acknowledgments

We thank LokLun Shek and Candy Lam for helping to collect the water samples and physical-chemical parameters and Mingming Sun for her help with 454 pyrosequencing preparation. This research is supported by the University Grants Committee (UGC) Areas of Excellence Scheme (AoE/P-04/04); the Research Grants Council’s GRF grants (661610, 661911, and 661912); and the Department of Agriculture, Fishery, and Conservation (AFCD) of Hong Kong SAR under contract AFCD08-07 L04810/11PG.

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Rocke, E., Jing, H., Xia, X. et al. Effects of Hypoxia on the Phylogenetic Composition and Species Distribution of Protists in a Subtropical Harbor. Microb Ecol 72, 96–105 (2016). https://doi.org/10.1007/s00248-016-0751-7

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