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The Ecology of One Cosmopolitan, One Newly Introduced and One Occasionally Advected Species from the Genus Skeletonema in a Highly Structured Ecosystem, the Northern Adriatic

Microbial Ecology volume 75, pages 674–687 (2018)Cite this article

Abstract

The diatom genus Skeletonema is globally distributed and often an important constituent of the phytoplankton community. In the marine phytoplankton of the northern Adriatic Sea, we found three species of the genus Skeletonema: Skeletonema menzelii, Skeletonema marinoi and Skeletonema grevillei. Making use of the steep ecological gradients that characterise the northern Adriatic, along which we could observe those species, we report here on the ecological circumstances under which those species thrive and how their respective populations are globally connected. This is the first detailed ecological study for the species S. grevillei. This study is also the first report for S. grevillei for the Adriatic Sea and Mediterranean together with additional electron microscopic details on fresh in situ samples for this species. S. marinoi appears to clearly prefer strong freshwater influence and high nutrient concentrations delivered by low salinity waters. It can outcompete other diatom species and dominate microphytoplankton blooms. S. grevillei on the other hand appears to thrive in high nutrient concentrations triggered by water column mixing. It also appears to prefer higher salinity waters and coastal embayments. Genetic analysis of S. grevillei demonstrated a peculiar dissimilarity with isolates from coastal waters off Yemen, India, Oman and China. However, a closely related sequence was isolated from coastal waters off Japan. These results indicate that S. grevillei is an introduced species, possibly transported by ballast waters. S. menzelii is a sporadic visitor in the northern Adriatic, advected from rather oligotrophic middle Adriatic waters and never dominates the phytoplankton community in the northern Adriatic.

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Abbreviations

FP:

Fultoportula

FPP:

Fultoportula process

IFPP:

Intercalary fultoportula process

IRP:

Intercalary rimoportula

IRPP:

Intercalary rimoportula process

RP:

Rimoportula

RPP:

Rimoportula process

TFP:

Terminal fultoportula

TFPP:

Terminal fultoportula process

TRP:

Terminal rimoportula

TRPP:

Terminal rimoportula process

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Acknowledgements

We are grateful for the work of Jasna Jakovcevic, Denis Skalic and Margareta Buterer in ocean sampling and in the analysis of oceanographic parameters as well as in database handling. This work was supported by the Ministry of Science, Education and Sports of the Republic of Croatia as well as by the scientific project UIP-2014-09-6563 (Phytoplankton life strategies in the northern Adriatic), funded by the Croatian Science Foundation as well as by the EU SYNTHESYS projects DE-TAF-4090 and DE-TAF-4112. D.M.P. is grateful to teachers and colleagues from the 11th Advanced Phytoplankton Course where these results were discussed for the first time. We are grateful to two anonymous reviewers for their insightful improvements of the manuscript.

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Authors and Affiliations

  1. Ruđer Bošković Institute, Center for Marine Research, G. Paliaga 5, HR-52210, Rovinj, Croatia

    Daniela Marić Pfannkuchen, Mirta Smodlaka Tanković, Ana Baričević, Nataša Kužat, Tamara Djakovac & Martin Pfannkuchen

  2. Division for Marine and Environmental Research, Ruđer Bošković Institute, Bijenička cesta 54, Zagreb, Croatia

    Jelena Godrijan

  3. Department for Natural and Health Sciences, Juraj Dobrila University of Pula, Zagrebačka 30, HR-52100, Pula, Croatia

    Emina Pustijanac

  4. Botanischer Garten und Botanisches Museum Berlin-Dahlem, Freie Universität Berlin, Königin-Luise-Str.6-8, Berlin, Germany

    Regina Jahn

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  1. Daniela Marić Pfannkuchen
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Correspondence to Martin Pfannkuchen.

Electronic Supplementary Material

Supplementary Fig. 1

Micrographs of S. marinoi from culture material. a Light micrograph of the colony. Scale bar, 20 μm. b Colony in girdle view at SEM. Scale bar, 10 μm. c Terminal valve of the colony with the long marginal TRPP showing flared ends of TFPPs with dentate margins. Scale bar, 10 μm. d Terminal valve of the colony with subcentral TRPP (arrow). Scale bar, 3 μm. e Intercalary valves with the IFPP connected with 1:1 plain joins or zigzag (arrow). Scale bar, 2 μm. f Intercalary valve with ridges between IFPP bases and a small IRPP (arrow). Scale bar, 3 μm. g Detail of an intercalary valves with several joining the IFPP. Scale bar, 2 μm. h Cingular bands with the transversal ribs. Scale bar, 1 μm. (JPEG 236 kb)

Supplementary Fig. 2

Correlation plot between concomitantly observed abundances of S. marinoi (a), S. grevillei (b) and total microphytoplankton, total diatoms (BACI), total dinoflagellates (DINO) and total coccolithophorids (COCCO). Numbers given are correlation coefficients. ***P < 0.001; **P < 0.01; *P < 0.05. (JPEG 113 kb)

Supplementary Fig. 3

a Neighbour-joining representation of sequences of S. grevillei covering the D1–D3 region of the LSU rDNA. b Neighbour-joining tree representation of sequences of S. grevillei covering the V4 region of the SSU rDNA. Isolates from the northern Adriatic are marked with an arrow. (JPEG 210 kb)

Supplementary Fig. 4

Genetic distances between all analysed isolates of S. grevillei. Marker gene: D1–D3 region of the LSU rDNA. (JPEG 439 kb) (JPEG 439 kb)

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Marić Pfannkuchen, D., Godrijan, J., Smodlaka Tanković, M. et al. The Ecology of One Cosmopolitan, One Newly Introduced and One Occasionally Advected Species from the Genus Skeletonema in a Highly Structured Ecosystem, the Northern Adriatic. Microb Ecol 75, 674–687 (2018). https://doi.org/10.1007/s00248-017-1069-9

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Keywords

  • Phytoplankton
  • Northern Adriatic
  • Diatoms
  • Skeletonema marinoi
  • Skeletonema grevillei