Advertisement

Polar Biology

, Volume 39, Issue 10, pp 1749–1763 | Cite as

Springtime dynamics, productivity and activity of prokaryotes in two Arctic fjords

  • A. M.-T. Piquet
  • D. S. Maat
  • V. Confurius-Guns
  • E. Sintes
  • G. J. Herndl
  • W. H. van de Poll
  • C. Wiencke
  • A. G. J. Buma
  • H. Bolhuis
Original Paper

Abstract

In the Kongsfjorden–Krossfjorden system (Spitsbergen), increasing temperatures enhance glacier melting and concomitant intrusion of freshwater. These altered conditions affect the timing, intensity, and composition of the phytoplankton spring bloom in Kongsfjorden; yet, the effects on prokaryotes (bacteria and archaea) are not well understood. The aim of this study was to examine springtime prokaryote communities in both fjords as a function of hydrographic and phytoplankton variability. Prokaryote community composition was studied in two consecutive years by molecular fingerprinting of the 16S rRNA gene. In addition, we measured bacterial abundance, productivity (3H-Leucine uptake), and single-cell activity using catalyzed reporter deposition fluorescence in situ hybridization combined with microautoradiography. Differences in bacterial and archaeal communities were found between Kongsfjorden and Krossfjorden. Furthermore, an increase in productivity, abundance, and proportion of active bacterial cells was observed during the course of spring. Bacteroidetes were the most abundant bacterial group among the assessed taxa in both Kongsfjorden and Krossfjorden. Multivariate analysis of the microbial community fingerprints revealed a strong temporal shaping of both the bacterial and archaeal communities in addition to a spatial separation between the two fjords. A significant part of the observed bacterial variation could be explained by cyanobacterial biomass, as deduced from pigment analysis, and by phosphate concentration. Archaea were mainly controlled by abiotic factors. We speculate that the bacterial response to hydrographic changes and glacier meltwater is mediated through shifts in phytoplankton abundance and composition, whereas archaea are directly influenced by abiotic environmental variables.

Keywords

Polar Spitsbergen Bacteria Archaea Glacier melting Spring bloom Bacterial production Micro-CARD-FISH 

Notes

Acknowledgments

This research was financed by NWO, as part of the IPY–PAME framework. Fieldwork at Koldeway station was supported and financed by the AWI. We thank A. K. Olstad, captain of the RV Teisten, and E. Austerheim, Kings Bay laboratory manager, for the wonderful collaboration. We are grateful to R. J. W. Visser for collecting the 2007 samples and running phytoplankton pigment analyses. Nutrients were analyzed at the NIOZ by J. van Ooijen. We also acknowledge Michael Greenacre (Universitat Pompeu Fabra, Barcelona, Spain) for his valuable help with the ordination and statistical analysis. We also like to thank the anonymous referees for their valuable suggestions and improvements.

References

  1. Alonso-Sáez L, Sánchez O, Gasol JM, Balagué V, Pedrós-Alió C (2008) Winter-to-summer changes in the composition and single-cell activity of near surface Arctic prokaryotes. Environ Microbiol 10:2444–2454CrossRefPubMedGoogle Scholar
  2. Alonso-Sáez L, Waller AS, Mende DR, Bakker K, Farnelid H, Yager PL et al (2012) Role for urea in nitrification by polar marine Archaea. Proc Natl Acad Sci USA 109:17989–17994CrossRefPubMedPubMedCentralGoogle Scholar
  3. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925PubMedPubMedCentralGoogle Scholar
  4. Amann RI, Ludwig W, Schleifer K (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169PubMedPubMedCentralGoogle Scholar
  5. Amin SA, Parker MS, Armbrust EV (2012) Interactions between diatoms and bacteria. Microbiol Mol Biol Rev 76:667–684CrossRefPubMedPubMedCentralGoogle Scholar
  6. Arnosti C (2008) Functional differences between Arctic seawater and sedimentary microbial communities: contrasts in microbial hydrolysis of complex substrates. FEMS Microbiol Ecol 66:343–351CrossRefPubMedGoogle Scholar
  7. Bano N, Hollibaugh JT (2002) Phylogenetic composition of bacterioplankton assemblages from the Arctic Ocean. Appl Environ Microbiol 68:505–518CrossRefPubMedPubMedCentralGoogle Scholar
  8. Brinkmeyer R, Knittel K, Jürgens J, Weyland H, Amann RI, Helmke E (2003) Diversity and structure of bacterial communities in Arctic versus Antarctic pack ice. Appl Environ Microbiol 69:6610–6619CrossRefPubMedPubMedCentralGoogle Scholar
  9. Brinkmeyer R, Glöckner F-O, Helmke E, Amann R (2004) Predominance of betaproteobacteria in summer melt pools on Arctic pack ice. Limnol Oceanogr 49:1013–1021CrossRefGoogle Scholar
  10. Collins RE, Rocap G, Deming JW (2010) Persistence of bacterial and archaeal communities in sea ice through an Arctic Winter. Environ Microbiol 12:1828–1841CrossRefPubMedPubMedCentralGoogle Scholar
  11. Comeau AM, Li WKW, Tremblay J, Carmack EC, Lovejoy C (2011) Arctic Ocean microbial community structure before and after the 2007 record sea ice minimum. PLoS One 6:e27492CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cottier F, Tverberg V, Inall M, Svendsen H, Nilsen F, Griffiths C (2005) Water mass modification in an Arctic fjord through cross-shelf exchange: the seasonal hydrography of Kongsfjorden, Svalbard. J Geophys Res C 110:1–18CrossRefGoogle Scholar
  13. Coupel P, Jin HY, Joo M, Horner R, Bouvet HA, Sicre M et al (2012) Phytoplankton distribution in unusually low sea ice cover over the Pacific Arctic. Biogeosciences 9:4835–4850CrossRefGoogle Scholar
  14. Daims H, Bruhl A, Amann R, Schleifer K, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444CrossRefPubMedGoogle Scholar
  15. Daufresne M, Lengfellner K, Sommer U (2009) Global warming benefits the small in aquatic ecosystems. P Natl Acad Sci USA 106:12788–12793CrossRefGoogle Scholar
  16. De Corte D, Sintes E, Yokokawa T, Herndl GJ (2011) Changes in viral and bacterial communities during the ice-melting season in the coastal Arctic (Kongsfjorden, Ny-Alesund). Environ Microbiol 13:1827–1841CrossRefPubMedGoogle Scholar
  17. De Corte D, Sintes E, Yokokawa T, Herndl GJ (2013) Comparison between MICRO-CARD-FISH and 16S rRNA gene clone libraries to assess the active versus total bacterial community in the coastal Arctic. Environ Microbiol Rep 5:272–281CrossRefPubMedGoogle Scholar
  18. Duarte CM, Agustí S, Wassmann P, Arrieta JM, Alcaraz M, Coello A, Marbà N et al (2012) Tipping elements in the Arctic marine ecosystem. Ambio 41:44–55CrossRefPubMedPubMedCentralGoogle Scholar
  19. Eilers H, Pernthaler J, Glockner F, Amann R (2000) Culturability and in situ abundance of pelagic bacteria from the North Sea. Appl Environ Microbiol 66:3044–3051CrossRefPubMedPubMedCentralGoogle Scholar
  20. Eilers H, Pernthaler J, Peplies J, Glockner F, Gerdts G, Amann R (2001) Isolation of novel pelagic bacteria from the German bight and their seasonal contributions to surface picoplankton. Appl Environ Microbiol 67:5134–5142CrossRefPubMedPubMedCentralGoogle Scholar
  21. Elifantz H, Dittel AI, Cottrell MT, Kirchman DL (2007) Dissolved organic matter assimilation by heterotrophic bacterial groups in the western Arctic Ocean. Aquat Microb Ecol 50:39–49CrossRefGoogle Scholar
  22. Galand PE, Lovejoy C, Pouliot J (2008) Microbial community diversity and heterotrophic production in a coastal Arctic ecosystem: a stamukhi lake and its source waters. Limnol Oceanogr 53:813–823CrossRefGoogle Scholar
  23. Garneau M, Vincent WF, Alonso-Sáez L, Gratton Y, Lovejoy C (2005) Prokaryotic community structure and heterotrophic production in a river-influences coastal arctic ecosystem. Aquat Microb Ecol 42:27–40CrossRefGoogle Scholar
  24. Glöckner FO, Fuchs BM, Amann RI (1999) Bacterioplankton composition of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65:3721–3726PubMedPubMedCentralGoogle Scholar
  25. Gonzalez J, Simo R, Massana R, Covert J, Casamayor E, Pedrós-Alió C et al (2000) Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom. Appl Environ Microbiol 66:4237–4246CrossRefPubMedPubMedCentralGoogle Scholar
  26. Greenacre M (2007) Correspondence analysis in practice, 2nd edn. Chapman & Hall/CRC, Boca RatonCrossRefGoogle Scholar
  27. Groudieva T, Kambourova M, Yusef H, Royter M, Grote R, Trinks H, Antranikian G (2004) Diversity and cold-active hydrolytic enzymes of culturable bacteria associated with Arctic sea ice, Spitzbergen. Extremophiles 8:475–488CrossRefPubMedGoogle Scholar
  28. Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeont Electr 4:38–47Google Scholar
  29. Hegseth EN, Tverberg V (2013) Effect of Atlantic water inflow on timing of the phytoplankton spring bloom in a high Arctic fjord (Kongsfjorden, Svalbard). J Marine Syst 113–114:94–105CrossRefGoogle Scholar
  30. Heuer H, Krsek M, Baker P, Smalla K, Wellington E (1997) Analysis of Actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63:3233–3241PubMedPubMedCentralGoogle Scholar
  31. Hodal H, Falk-Peterson S, Hop H, Kristiansen S, Reigstad M (2012) Spring bloom dynamics in Kongsfjorden, Svalbard: nutrients, phytoplankton, protozoans and primary production. Polar Biol 35:191–203CrossRefGoogle Scholar
  32. Hop H, Pearson T, Hegseth EN, Kovacs KM, Wiencke C, Kwasniewski S et al (2002) The marine ecosystem of Kongsfjorden, Svalbard. Polar Res 21:167–208CrossRefGoogle Scholar
  33. Keck A, Wiktor J, Hapter R, Nilsen R (1999) Phytoplankton assemblages related to physical gradients in an arctic, glacier-fed fjord in summer. ICES J Mar Sci 56:203–214CrossRefGoogle Scholar
  34. Kellogg C, Deming JW (2009) Comparison of free-living, suspended particle and aggregate-associated bacterial and archaeal communities in the Laptev Sea. Aquat Microb Ecol 57:1–18CrossRefGoogle Scholar
  35. Kirchman DL (2002) The ecology of CytophagaFlavobacteria in aquatic environments. FEMS Microbiol Ecol 39:91–100PubMedGoogle Scholar
  36. Kirchman DL (2008) New light on an important microbe in the ocean. P Natl Acad Sci USA 105:8487–8488CrossRefGoogle Scholar
  37. Kirchman DL, Ducklow HW (1993) Estimating conversion factors for the thymidine and leucine methods for measuring bacterial production. In: Kemp PF, Cole JJ, Sherr BF, Sherr BE (eds) Handbook of methods in aquatic microbial ecology. CRC Press, New York, pp 513–519Google Scholar
  38. Kirchman DL, Dittel A, Malmstrom R, Cottrell M (2005) Biogeography of major bacterial groups in the Delaware Estuary. Limnol Oceanogr 50:1697–1706CrossRefGoogle Scholar
  39. Kirchman DL, Elifantz H, Dittel AI, Malmstrom RR, Cottrell MT (2007) Standing stocks and activity of Archaea and Bacteria in the Western Arctic Ocean. Limnol Oceanogr 52:495–507CrossRefGoogle Scholar
  40. Lee N, Nielsen P, Andreasen K, Juretschko S, Nielsen J, Schleifer K et al (1999) Combination of fluorescent in situ hybridization and microautoradiography: a new tool for structure-function analyses in microbial ecology. Appl Environ Microbiol 65:1289–1297PubMedPubMedCentralGoogle Scholar
  41. Leu E, Falk-Peterson S, Kwasniewski S, Wulff A, Edvardson K, Hessen DO (2006) Fatty acid dynamics during the spring bloom in a high Arctic fjord: importanc of abiotic factors versus community changes. Can J Fish Aquat Sci 63:2760–2779CrossRefGoogle Scholar
  42. Li WKW, McLaughlin FA, Lovejoy C, Carmack EC (2009) Smallest algae thrive as the Arctic Ocean freshens. Science 326:539CrossRefPubMedGoogle Scholar
  43. Malmstrom RR, Straza TRA, Cotrell MT, Kirchman DL (2007) Diversity, abundance, and biomass production of bacterial groups in the western Arctic Ocean. Aquat Microb Ecol 47:45–55CrossRefGoogle Scholar
  44. Manz W, Amann R, Ludwig W, Wagner M, Schleifer K (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria: problems and solutions. Syst Appl Microbiol 15:593–600CrossRefGoogle Scholar
  45. Manz W, Amann R, Ludwig W, Vancanneyt M, Schleifer K (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga–flavobacter–bacteroides in the natural environment. Microbiology 142:1097–1106CrossRefPubMedGoogle Scholar
  46. Moline M, Claustre H, Frazer T, Schofield O, Vernet M (2004) Alteration of the food web along the Antarctic Peninsula in response to a regional warming trend. Global Change Biol 10:1973–1980CrossRefGoogle Scholar
  47. Morris R, Rappe M, Connon S, Vergin K, Siebold W, Carlson C et al (2002) SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420:806–810CrossRefPubMedGoogle Scholar
  48. Murray AE, Preston CM, Massana R, Taylor LT, Blakis A, Wu K et al (1998) Seasonal and spatial variability of bacterial and Archaeal assemblages in coastal waters near Anvers Island, Antarctica. Appl Environ Microbiol 64:2585–2595PubMedPubMedCentralGoogle Scholar
  49. Nicol GW, Glover LA, Prosser JI (2003) Molecular analysis of methanogenic archaeal communities in managed and natural upland pasture soils. Glob Change Biol 9:1451–1457CrossRefGoogle Scholar
  50. Oksanen J, Blanchet GF, Kindt R, Legendre P, Minchin PR, O’Hara RB et al. (2014) Vegan: community ecology package. R package version 2.2-0Google Scholar
  51. Olsen MS, Callaghan TV, Reist JD, Reiersen LO, Dahl-Jensen D, Granskog MA et al (2011) The changing arctic cryosphere and likely consequences: an overview. Special report: Arctic cryosphere: changes and impacts. Ambio 40(1):111–118Google Scholar
  52. Ortega-Retuerta E, Reche E, Pulido-Villena E, Agustí S, Duarte CM (2008) Exploring the relationship between active bacterioplankton and phytoplankton in the Southern Ocean. Aquat Microb Ecol 52:99–106CrossRefGoogle Scholar
  53. Osterholz H, Dittmar T, Niggemann J (2014) Molecular evidence for rapid dissolved organic matter turnover in Arctic fjords. Mar Chem 160:1–10CrossRefGoogle Scholar
  54. Ovreas L, Forney L, Daae F, Torsvik V (1997) Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63:3367–3373PubMedPubMedCentralGoogle Scholar
  55. Pernthaler A, Pernthaler J, Amann R (2002a) Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Environ Microbiol 68:3094–3101CrossRefPubMedPubMedCentralGoogle Scholar
  56. Pernthaler A, Preston C, Pernthaler J, DeLong E, Amann R (2002b) Comparison of fluorescently labeled oligonucleotide and polynucleotide probes for the detection of pelagic marine bacteria and archaea. Appl Environ Microbiol 68:661–667CrossRefPubMedPubMedCentralGoogle Scholar
  57. Piquet AM-T, Bolhuis H, Davidson AT, Thomson PG, Buma AGJ (2008) Diversity and dynamics of Antarctic marine microbial eukaryotes under manipulated environmental UV radiation. FEMS Microbiol Ecol 66:352–366CrossRefPubMedGoogle Scholar
  58. Piquet AM-T, Scheepens JF, Bolhuis H, Wiencke C, Buma AGJ (2010) Variability of protistan and bacterial communities in two Arctic fjords (Spitsbergen). Polar Biol 33:1521–1536CrossRefGoogle Scholar
  59. Piquet AM-T, van de Poll WH, Visser RJW, Wiencke C, Bolhuis H, Buma AGJ (2014) Springtime phytoplankton dynamics in Arctic Krossfjorden and Kongsfjorden (Spitsbergen) as a function of glacier proximity. Biogeosciences 11:2263–2279CrossRefGoogle Scholar
  60. Ravenschlag K, Sahm K, Pernthaler J, Amann R (1999) High bacterial diversity in permanently cold marine sediments. Appl Environ Microbiol 65:3982–3989PubMedPubMedCentralGoogle Scholar
  61. Riemann L, Steward G, Azam F (2000) Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Appl Environ Microbiol 66:578–587CrossRefPubMedPubMedCentralGoogle Scholar
  62. Rokkan Iversen K, Seuthe L (2011) Seasonal microbial processes in a high-latitude fjord (Kongsfjorden, Svalbard): I. Heterotrophic bacteria, picoplankton and nanoflagellates. Polar Biol 34:731–749CrossRefGoogle Scholar
  63. Sala MM, Terrado R, Lovejoy C, Unrein F, Pedrós-Alió C (2008) Metabolic diversity of heterotrophic bacterioplankton over winter and spring in the coastal Arctic Ocean. Environ Microbiol 10:942–949CrossRefPubMedGoogle Scholar
  64. Seuthe L, Topper B, Reigstad M, Thyrhaug R, Vaquer-Sunyer R (2011) Microbial communities and processes in ice-covered Arctic waters of the northwestern Fram Strait (75 to 80 degrees N) during the vernal pre-bloom phase. Aquat Microb Ecol 64:253–266CrossRefGoogle Scholar
  65. Simon M, Azam F (1989) Protein content and protein synthesis rates of planktonic marine Bacteria. Mar Ecol Prog Ser 51:201–213CrossRefGoogle Scholar
  66. Smith DC, Azam F (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microb Food Webs 6:107–114Google Scholar
  67. Srinivas TNR, Nageswara Rao SSS, Vishnu Vardhan Reddy P, Pratibha MS, Sailaja B, Kavya B et al (2009) Bacterial diversity and bioprospecting for cold-active lipases, amylases and proteases, from culturable bacteria of Kongsfjorden and Ny-Ålesund, Svalbard, Arctic. Curr Microbiol 59:537–547CrossRefPubMedGoogle Scholar
  68. Svendsen H, Beszczynska-Møller A, Hagen JO, Lefauconnier B, Tverberg V, Gerland S et al (2002) The physical environment of the Kongsfjorden–Krossfjorden, an arctic fjord system in Svalbard. Polar Res 21:133–166CrossRefGoogle Scholar
  69. Tian F, Yu Y, Chen B, Li H, Yao Y-F, Guo X-K (2009) Bacterial, archaeal and eukaryotic diversity in Arctic sediment as revealed by 16S rRNA and 18S rRNA gene clone libraries analysis. Polar Biol 32:93–103CrossRefGoogle Scholar
  70. Teira E, Reinthaler T, Pernthaler A, Pernthaler J, Herndl GJ (2004) Combining catalyzed reporter deposition-fluorescence in situ hybridization and microautoradiography to detect substrate utilization by bacteria and archaea in the deep ocean. Appl Environ Microbiol 70:4411–4414CrossRefPubMedPubMedCentralGoogle Scholar
  71. van der Wielen P, Bolhuis H, Borin S, Daffonchio D, Corselli C, Giuliano L et al (2005) The enigma of prokaryotic life in deep hypersaline anoxic basins. Science 307:121–123CrossRefPubMedGoogle Scholar
  72. Vincent WF, Callaghan TV, Dahl-Jensen D, Johansson M, Kovacs KM, Michel C, Prowse T, Reist JD, Sharp M (2011) Ecological implications of changes in the Arctic cryosphere. Ambio 40:87–99CrossRefGoogle Scholar
  73. Zeng Y, Zheng T, Li H (2009) Community composition of the marine bacterioplankton in Kongsfjorden (Spitsbergen) as revealed by 16S rRNA gene analysis. Polar Biol 32:1447–1460CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • A. M.-T. Piquet
    • 1
  • D. S. Maat
    • 2
  • V. Confurius-Guns
    • 3
  • E. Sintes
    • 4
  • G. J. Herndl
    • 2
    • 4
  • W. H. van de Poll
    • 1
  • C. Wiencke
    • 5
  • A. G. J. Buma
    • 1
    • 6
  • H. Bolhuis
    • 3
  1. 1.Department of Ocean Ecosystems, Energy and Sustainability Research Institute GroningenUniversity of GroningenGroningenThe Netherlands
  2. 2.Department of Biological OceanographyRoyal Netherlands Institute for Sea ResearchDen Burg, TexelThe Netherlands
  3. 3.Marine MicrobiologyRoyal Netherlands Institute for Sea ResearchYersekeThe Netherlands
  4. 4.Department of Limnology and Bio-OceanographyUniversity of ViennaViennaAustria
  5. 5.Department of Functional EcologyAlfred Wegener InstituteBremerhavenGermany
  6. 6.Arctic CentreUniversity of GroningenGroningenThe Netherlands

Personalised recommendations