Polar Biology

, Volume 42, Issue 1, pp 159–169 | Cite as

Summer phyto- and bacterioplankton communities during low and high productivity scenarios in the Western Antarctic Peninsula

  • Sebastián Fuentes
  • José Ignacio Arroyo
  • Susana Rodríguez-Marconi
  • Italo Masotti
  • Tomás Alarcón-Schumacher
  • Martin F. Polz
  • Nicole Trefault
  • Rodrigo De la Iglesia
  • Beatriz DíezEmail author
Original Paper


Phytoplankton blooms taking place during the warm season drive high productivity in Antarctic coastal seawaters. Important temporal and spatial variations exist in productivity patterns, indicating local constraints influencing the phototrophic community. Surface water in Chile Bay (Greenwich Island, South Shetlands) is influenced by freshwater from the melting of sea ice and surrounding glaciers; however, it is not a widely studied system. The phyto- and bacterioplankton communities in Chile Bay were studied over two consecutive summers; during a low productivity period (chlorophyll a < 0.05 mg m−3) and an ascendant phototrophic bloom (chlorophyll a up to 2.38 mg m−3). Microbial communities were analyzed by 16S rRNA—including plastidial—gene sequencing. Diatoms (mainly Thalassiosirales) were the most abundant phytoplankton, particularly during the ascendant bloom. Bacterioplankton in the low productivity period was less diverse and dominated by a few operational taxonomic units (OTUs), related to Colwellia and Pseudoalteromonas. Alpha diversity was higher during the bloom, where several Bacteroidetes taxa absent in the low productivity period were present. Network analysis indicated that phytoplankton relative abundance was correlated with bacterioplankton phylogenetic diversity and the abundance of several bacterial taxa. Hubs—the most connected OTUs in the network—were not the most abundant OTUs and included some poorly described taxa in Antarctica, such as Neptunomonas and Ekhidna. In summary, the results of this study indicate that in Antarctic Peninsula coastal waters, such as Chile Bay, higher bacterioplankton community diversity occurs during a phototrophic bloom. This is likely a result of primary production, providing a source of fresh organic matter to bacterioplankton.


Bacterioplankton Phytoplankton Antarctic Peninsula 16S rRNA gene sequencing 



The authors gratefully acknowledge the Armada de Chile staff at Arturo Prat Station and the staff from the Chilean Antarctic Institute (INACH); their support made possible the sampling in Chile Bay. The authors also thank the Department of Climatology, Centro Meteorológico de Valparaíso, Armada de Chile, for the meteorological data and María Estrella Alcamán, Cynthia Sanhueza, Laura Farías and Josefa Verdugo for their assistance with sample collection.


This work was financially supported by the grants INACH15-10, INACH_RG_09_17, CONICYT for international cooperation DPI20140044, FONDAP N°15110009, FONDECYT postdoctoral N°3160424, CONICYT PhD scholarship N°21130515 and CONICYT magister scholarship N°22172113.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involved in human and animal rights

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

300_2018_2411_MOESM1_ESM.pdf (135 kb)
Supplementary material 1 (PDF 135 kb)
300_2018_2411_MOESM2_ESM.pdf (273 kb)
Supplementary material 2 (PDF 272 kb)
300_2018_2411_MOESM3_ESM.pdf (1.8 mb)
Supplementary material 3 (PDF 1799 kb)
300_2018_2411_MOESM4_ESM.pdf (1.5 mb)
Supplementary material 4 (PDF 1573 kb)


  1. Alain K, Tindall BJ, Catala P et al (2010) Ekhidna lutea gen. nov., sp. nov., a member of the phylum Bacteroidetes isolated from the South East Pacific Ocean. Int J Syst Evol Microbiol 60:2972–2978. CrossRefGoogle Scholar
  2. Allen A, Gillooly J, Brown J (2007) Recasting the species-energy hypothesis: the different roles of kinetic and potential energy in regulating biodiversity. In: Storch D, Marquet P, Brown J (eds) Scaling biodiversity. Cambridge University Press, Cambridge, pp 283–299CrossRefGoogle Scholar
  3. Allers E, Niesner C, Wild C, Pernthaler J (2008) Microbes enriched in seawater after addition of coral mucus. Appl Environ Microbiol 74:3274–3278. CrossRefGoogle Scholar
  4. Almandoz GO, Ferreyra GA, Schloss IR et al (2008) Distribution and ecology of Pseudo-nitzschia species (Bacillariophyceae) in surface waters of the Weddell Sea (Antarctica). Polar Biol 31:429–442. CrossRefGoogle Scholar
  5. Amaro AM, Fuentes MS, Ogalde SR et al (2005) Identification and characterization of potentially algal-lytic marine bacteria strongly associated with the toxic dinoflagellate Alexandrium catenella. J Eukaryot Microbiol 52:191–200. CrossRefGoogle Scholar
  6. Barberán A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6:343–351. CrossRefGoogle Scholar
  7. Bar-Massada A (2015) Complex relationships between species niches and environmental heterogeneity affect species co-occurrence patterns in modelled and real communities. Proc R Soc Biol Sci 282:20150927. CrossRefGoogle Scholar
  8. Borges Mendes CR, Silva de Souza M, Tavano Garcia VM et al (2012) Dynamics of phytoplankton communities during late summer around the tip of the Antarctic Peninsula. Deep Res Part I Oceanogr Res Pap 65:1–14. CrossRefGoogle Scholar
  9. Buchan A, LeCleir GR, Gulvik CA, Gonzalez JM (2014) Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol 12:686–698. CrossRefGoogle Scholar
  10. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. CrossRefGoogle Scholar
  11. Cavicchioli R (2015) Microbial ecology of Antarctic aquatic systems. Nat Rev Microbiol 13:691–706. CrossRefGoogle Scholar
  12. Chorus I, Bartram J (1999) Toxic cyanobacteria in water. A guide to their public health consequences, monitoring and management. World Health Organization, CRC Press, Boca RatonCrossRefGoogle Scholar
  13. Decelle J, Romac S, Stern RF et al (2015) PhytoREF: a reference database of the plastidial 16S rRNA gene of photosynthetic eukaryotes with curated taxonomy. Mol Ecol Resour 15:1435–1445. CrossRefGoogle Scholar
  14. Delmont TO, Hammar KM, Ducklow HW et al (2014) Phaeocystis antarctica blooms strongly influence bacterial community structures in the Amundsen Sea polynya. Front Microbiol 5:1–13. CrossRefGoogle Scholar
  15. Díez B, Pedrós-Alió C, Massana R (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. CrossRefGoogle Scholar
  16. Dinasquet J, Richert I, Logares R et al (2017) Mixing of water masses caused by a drifting iceberg affects bacterial activity, community composition and substrate utilization capability in the Southern Ocean. Environ Microbiol 19:2453–2467. CrossRefGoogle Scholar
  17. DiTullio GR, Grebmeier JM, Arrigo KR et al (2000) Rapid and early export of Phaeocystis antarctica blooms in the Ross Sea, Antarctica. Nature 404:595–598. CrossRefGoogle Scholar
  18. Ducklow H, Fraser W, Meredith M et al (2013) West Antarctic Peninsula: an ice-dependent coastal marine ecosystem in transition. Oceanography 26:190–203. CrossRefGoogle Scholar
  19. Durkin CA, Mock T, Armbrust EV (2009) Chitin in diatoms and its association with the cell wall. Eukaryot Cell 8:1038–1050. CrossRefGoogle Scholar
  20. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. CrossRefGoogle Scholar
  21. Egas C, Henríquez-Castillo C, Delherbe N et al (2017) Short timescale dynamics of phytoplankton in Fildes Bay, Antarctica. Antarct Sci 29:1–12. CrossRefGoogle Scholar
  22. Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. CrossRefGoogle Scholar
  23. Fernández-Gómez B, Richter M, Schuler M et al (2013) Ecology of marine Bacteroidetes: a comparative genomics approach. ISME J 7:1026–1037. CrossRefGoogle Scholar
  24. Garibotti IA, Vernet M, Ferrario ME (2005) Annually recurrent phytoplanktonic assemblages during summer in the seasonal ice zone west of the Antarctic Peninsula (Southern Ocean). Deep Res Part I Oceanogr Res Pap 52:1823–1841. CrossRefGoogle Scholar
  25. Ghiglione J-F, Murray AE (2012) Pronounced summer to winter differences and higher wintertime richness in coastal Antarctic marine bacterioplankton. Environ Microbiol 14:617–629. CrossRefGoogle Scholar
  26. Gonçalves-Araujo R, Silva de Souza M, Tavano VM, Eiras Garcia CA (2015) Influence of oceanographic features on spatial and interannual variability of phytoplankton in the Bransfield Strait, Antarctica. J Mar Syst 142:1–15. CrossRefGoogle Scholar
  27. Gutt J, Adams B, Bracegirdle T et al (2012) Antarctic thresholds—Ecosystem resilience and adaptation: a new SCAR-biology programme. Polarforschung 82:147–150Google Scholar
  28. Handayani M, Sasaki H, Matsuda R et al (2014) Characterization of an epiphytic bacterium Neptunomonas sp. BPy-1 on the gametophytes of a red alga pyropia yezoensis. Am J Plant Sci 5:3652–3661. CrossRefGoogle Scholar
  29. Landaeta MF, Vera-Duarte J, Manríquez K et al (2017) Trophic plasticity of larval notothenioid fish Harpagifer antarcticus in shallow waters from the South Shetland Islands, Antarctica. Polar Biol 40:837–851. CrossRefGoogle Scholar
  30. Lovejoy C, Bowman JP, Hallegraeff GM (1998) Algicidal effects of a novel marine Pseudoalteromonas isolate (class Proteobacteria, Gamma subdivision) on harmful algal bloom species of the genera Chattonella, Gymnodinium, and Heterosigma. Appl Environ Microbiol 64:2806–2813Google Scholar
  31. Luria C, Amaral-Zettler L, Ducklow H, Rich J (2016) Seasonal succession of bacterial communities in coastal waters of the western Antarctic Peninsula. Front Microbiol 7:1731. CrossRefGoogle Scholar
  32. Milici M, Vital M, Tomasch J et al (2017) Diversity and community composition of particle-associated and free-living bacteria in mesopelagic and bathypelagic Southern Ocean water masses: evidence of dispersal limitation in the Bransfield Strait. Limnol Oceanogr 62:1080–1095. CrossRefGoogle Scholar
  33. Nedashkovskaya OI, Kim SB, Han SK et al (2004) Ulvibacter litoralis gen. nov., sp. nov., a novel member of the family Flavobacteriaceae isolated from the green alga Ulva fenestrata. Int J Syst Evol Microbiol 54:119–123. CrossRefGoogle Scholar
  34. Piquet AMT, Bolhuis H, Davidson AT et al (2008) Diversity and dynamics of Antarctic marine microbial eukaryotes under manipulated environmental UV radiation. FEMS Microbiol Ecol 66:352–366. CrossRefGoogle Scholar
  35. Piquet AMT, Bolhuis H, Meredith MP, Buma AGJ (2011) Shifts in coastal Antarctic marine microbial communities during and after melt water-related surface stratification. FEMS Microbiol Ecol 76:413–427. CrossRefGoogle Scholar
  36. Pons P, Latapy M (2006) Computing communities in large networks using random walks. J Graph Algorithms Appl 10:191–218. CrossRefGoogle Scholar
  37. Power ME, Tilman D, Estes JA et al (1996) Challenges in the quest for keystones. Bioscience 46:609–620. CrossRefGoogle Scholar
  38. Preheim SP, Perrotta AR, Martin-Platero AM et al (2013) Distribution-based clustering: using ecology to refine the operational taxonomic unit. Appl Environ Microbiol 79:6593–6603. CrossRefGoogle Scholar
  39. Prézelin BB, Hofmann EE, Mengelt C, Klinck John M (2000) The linkage between Upper Circumpolar DeepWater (UCDW) and phytoplankton assemblages on the west Antarctic Peninsula continental shelf. J Mar Res 58:165–202. CrossRefGoogle Scholar
  40. Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596. CrossRefGoogle Scholar
  41. Rideout JR, He Y, Navas-Molina JA et al (2014) Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences. PeerJ 2:e545. CrossRefGoogle Scholar
  42. Riemann L, Steward GF, Azam F (2000) Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Appl Environ Microbiol 66:578–587. CrossRefGoogle Scholar
  43. Sala MM, Terrado R, Lovejoy C et al (2008) Metabolic diversity of heterotrophic bacterioplankton over winter and spring in the coastal Arctic Ocean. Environ Microbiol 10:942–949. CrossRefGoogle Scholar
  44. Schloss IR, Abele D, Moreau S et al (2012) Response of phytoplankton dynamics to 19-year (1991–2009) climate trends in Potter Cove (Antarctica). J Mar Syst 92:53–66. CrossRefGoogle Scholar
  45. Shannon P, Markiel A, Ozier O et al (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. CrossRefGoogle Scholar
  46. Stewart FJ, Dalsgaard T, Young CR et al (2012) Experimental incubations elicit profound changes in community transcription in OMZ bacterioplankton. PLoS ONE. Google Scholar
  47. Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis, 2nd edn. The Alger Press Ltd, OttawaGoogle Scholar
  48. Teeling H, Fuchs BM, Bennke CM et al (2016) Recurring patterns in bacterioplankton dynamics during coastal spring algae blooms. Elife 5:e11888. CrossRefGoogle Scholar
  49. Vernet M, Martinson D, Iannuzzi R et al (2008) Primary production within the sea-ice zone west of the Antarctic Peninsula: I - Sea ice, summer mixed layer, and irradiance. Deep Res Part II Top Stud Oceanogr 55:2068–2085. CrossRefGoogle Scholar
  50. West NJ, Obernosterer I, Zemb O, Lebaron P (2008) Major differences of bacterial diversity and activity inside and outside of a natural iron-fertilized phytoplankton bloom in the Southern Ocean. Environ Microbiol 10:738–756. CrossRefGoogle Scholar
  51. Wietz M, Wemheuer B, Simon H et al (2015) Bacterial community dynamics during polysaccharide degradation at contrasting sites in the Southern and Atlantic Oceans. Environ Microbiol 17:3822–3831. CrossRefGoogle Scholar
  52. Wilkins D, Yau S, Williams TJ et al (2013) Key microbial drivers in Antarctic aquatic environments. FEMS Microbiol Rev 37:303–335. CrossRefGoogle Scholar
  53. Wright DH (1983) Species-energy theory: an extension of species-area theory. Oikos 41:496–506CrossRefGoogle Scholar
  54. Zhang GI, Hwang CY, Kang SH, Cho BC (2009) Maribacter antarcticus sp. nov., a psychrophilic bacterium isolated from a culture of the Antarctic green alga Pyramimonas gelidicola. Int J Syst Evol Microbiol 59:1455–1459. CrossRefGoogle Scholar
  55. Zhao T, Liu H, Roeder K et al (2012) The huge package for high-dimensional undirected graph estimation in R. J Mach Learn Res 13:1059–1062Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Sebastián Fuentes
    • 1
    • 2
  • José Ignacio Arroyo
    • 1
    • 2
  • Susana Rodríguez-Marconi
    • 3
    • 4
  • Italo Masotti
    • 3
  • Tomás Alarcón-Schumacher
    • 1
    • 2
  • Martin F. Polz
    • 5
  • Nicole Trefault
    • 6
  • Rodrigo De la Iglesia
    • 1
  • Beatriz Díez
    • 1
    • 2
    Email author
  1. 1.Departament of Molecular Genetics and Microbiology, Faculty of Biological SciencesPontificia Universidad Católica de ChileSantiagoChile
  2. 2.Center for Climate and Resilience Research (CR)2SantiagoChile
  3. 3.Facultad de Ciencias del Mar y de Recursos Naturales, Universidad de ValparaísoViña del MarChile
  4. 4.Programa de Magister en OceanografíaUniversidad de Valparaíso - Pontificia Universidad Católica de ValparaísoValparaisoChile
  5. 5.Department of Civil and Environmental EngineeringMassachusetts Institute of TechnologyCambridgeUSA
  6. 6.Center for Genomics and Bioinformatics, Faculty of SciencesUniversidad MayorSantiagoChile

Personalised recommendations