A light-induced shortcut in the planktonic microbial loop

Robert Ptacnik; Ana Gomes; Sarah-Jeanne Royer; Stella A. Berger; Albert Calbet; Jens C. Nejstgaard; Josep M. Gasol; Stamatina Isari; Stefanie D. Moorthi; Radka Ptacnikova; Maren Striebel; Andrey F. Sazhin; Tatiana M. Tsagaraki; Soultana Zervoudaki; Kristi Altoja; Panagiotis D. Dimitriou; Peeter Laas; Ayse Gazihan; Rodrigo A. Martínez; Stefanie Schabhüttl; Ioulia Santi; Despoina Sousoni; Paraskevi Pitta

doi:10.1038/srep29286

A light-induced shortcut in the planktonic microbial loop

Robert Ptacnik, Ana Gomes, Sarah-Jeanne Royer, Stella A. Berger, Albert Calbet, Jens C. Nejstgaard, Josep M. Gasol, Stamatina Isari, Stefanie D. Moorthi, Radka Ptacnikova, Maren Striebel, Andrey F. Sazhin, Tatiana M. Tsagaraki, Soultana Zervoudaki, Kristi Altoja, Panagiotis D. Dimitriou, Peeter Laas, Ayse Gazihan, Rodrigo A. Martínez, Stefanie SchabhüttlIoulia Santi, Despoina Sousoni, Paraskevi Pitta

Biological, Environmental Sciences and Engineering

Research output: Contribution to journal › Article › peer-review

46 Scopus citations

Abstract

Mixotrophs combine photosynthesis with phagotrophy to cover their demands in energy and essential nutrients. This gives them a competitive advantage under oligotropihc conditions, where nutrients and bacteria concentrations are low. As the advantage for the mixotroph depends on light, the competition between mixo- and heterotrophic bacterivores should be regulated by light. To test this hypothesis, we incubated natural plankton from the ultra-oligotrophic Eastern Mediterranean in a set of mesocosms maintained at 4 light levels spanning a 10-fold light gradient. Picoplankton (heterotrophic bacteria (HB), pico-sized cyanobacteria, and small-sized flagellates) showed the fastest and most marked response to light, with pronounced predator-prey cycles, in the high-light treatments. Albeit cell specific activity of heterotrophic bacteria was constant across the light gradient, bacterial abundances exhibited an inverse relationship with light. This pattern was explained by light-induced top-down control of HB by bacterivorous phototrophic eukaryotes (PE), which was evidenced by a significant inverse relationship between HB net growth rate and PE abundances. Our results show that light mediates the impact of mixotrophic bacterivores. As mixo- and heterotrophs differ in the way they remineralize nutrients, these results have far-reaching implications for how nutrient cycling is affected by light.

Original language	English (US)
Journal	Scientific Reports
Volume	6
Issue number	1
DOIs	https://doi.org/10.1038/srep29286
State	Published - Jul 11 2016

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: The experiment was financed by the European Union Seventh Framework Program MESOAQUA (FP7/2009–2013) coordinated by JCN under grant agreement no. 228224. MESOAQUA granted Transnational Access to R. & R.P., S.D.M., M.S., S.S., A.G., K.A., P.L. (LightDynaMix), A.C., R.A.M., A.S., A.G., S.J.R., J.M.G. (LiMic) and S.I., S.Z. (LightCopFed). R.P. further acknowledges financial support by the German Research Council (DFG Pt 5/3-1), JMG by Spanish project REMEI (CTM2015-70340) and AC by project PROTOS (CTM2009-08783) from the Spanish Ministry of Economy and Competitiveness. T. Tanaka is highly acknowledged for contributing his data on phosphorus uptake and bacterial activity. The authors wish to thank Dr. P. Divanach for valuable advice on technical matters, G. Piperakis for his inspired technical assistance throughout the experiment, S. Zivanovic and E. Dafnomili for assistance with chemical analyses, D. Podaras for assistance during the experiment and N. Sekeris for his help with constructions and ideas. The captain and the crew of the R/V Philia are also thanked for their assistance during the transportation of water from the sea to the mesocosms. Comments by three anonymous reviewers have helped improving the manuscript.

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10.1038/srep29286

https://repository.kaust.edu.sa/bitstream/10754/617092/1/srep29286.pdf

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Ptacnik, R., Gomes, A., Royer, S.-J., Berger, S. A., Calbet, A., Nejstgaard, J. C., Gasol, J. M., Isari, S., Moorthi, S. D., Ptacnikova, R., Striebel, M., Sazhin, A. F., Tsagaraki, T. M., Zervoudaki, S., Altoja, K., Dimitriou, P. D., Laas, P., Gazihan, A., Martínez, R. A., ... Pitta, P. (2016). A light-induced shortcut in the planktonic microbial loop. Scientific Reports, 6(1). https://doi.org/10.1038/srep29286

@article{bf647cde1de04b89974c920d4b88c9ba,

title = "A light-induced shortcut in the planktonic microbial loop",

abstract = "Mixotrophs combine photosynthesis with phagotrophy to cover their demands in energy and essential nutrients. This gives them a competitive advantage under oligotropihc conditions, where nutrients and bacteria concentrations are low. As the advantage for the mixotroph depends on light, the competition between mixo- and heterotrophic bacterivores should be regulated by light. To test this hypothesis, we incubated natural plankton from the ultra-oligotrophic Eastern Mediterranean in a set of mesocosms maintained at 4 light levels spanning a 10-fold light gradient. Picoplankton (heterotrophic bacteria (HB), pico-sized cyanobacteria, and small-sized flagellates) showed the fastest and most marked response to light, with pronounced predator-prey cycles, in the high-light treatments. Albeit cell specific activity of heterotrophic bacteria was constant across the light gradient, bacterial abundances exhibited an inverse relationship with light. This pattern was explained by light-induced top-down control of HB by bacterivorous phototrophic eukaryotes (PE), which was evidenced by a significant inverse relationship between HB net growth rate and PE abundances. Our results show that light mediates the impact of mixotrophic bacterivores. As mixo- and heterotrophs differ in the way they remineralize nutrients, these results have far-reaching implications for how nutrient cycling is affected by light.",

author = "Robert Ptacnik and Ana Gomes and Sarah-Jeanne Royer and Berger, {Stella A.} and Albert Calbet and Nejstgaard, {Jens C.} and Gasol, {Josep M.} and Stamatina Isari and Moorthi, {Stefanie D.} and Radka Ptacnikova and Maren Striebel and Sazhin, {Andrey F.} and Tsagaraki, {Tatiana M.} and Soultana Zervoudaki and Kristi Altoja and Dimitriou, {Panagiotis D.} and Peeter Laas and Ayse Gazihan and Mart{\'i}nez, {Rodrigo A.} and Stefanie Schabh{\"u}ttl and Ioulia Santi and Despoina Sousoni and Paraskevi Pitta",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: The experiment was financed by the European Union Seventh Framework Program MESOAQUA (FP7/2009–2013) coordinated by JCN under grant agreement no. 228224. MESOAQUA granted Transnational Access to R. & R.P., S.D.M., M.S., S.S., A.G., K.A., P.L. (LightDynaMix), A.C., R.A.M., A.S., A.G., S.J.R., J.M.G. (LiMic) and S.I., S.Z. (LightCopFed). R.P. further acknowledges financial support by the German Research Council (DFG Pt 5/3-1), JMG by Spanish project REMEI (CTM2015-70340) and AC by project PROTOS (CTM2009-08783) from the Spanish Ministry of Economy and Competitiveness. T. Tanaka is highly acknowledged for contributing his data on phosphorus uptake and bacterial activity. The authors wish to thank Dr. P. Divanach for valuable advice on technical matters, G. Piperakis for his inspired technical assistance throughout the experiment, S. Zivanovic and E. Dafnomili for assistance with chemical analyses, D. Podaras for assistance during the experiment and N. Sekeris for his help with constructions and ideas. The captain and the crew of the R/V Philia are also thanked for their assistance during the transportation of water from the sea to the mesocosms. Comments by three anonymous reviewers have helped improving the manuscript.",

year = "2016",

month = jul,

day = "11",

doi = "10.1038/srep29286",

language = "English (US)",

volume = "6",

journal = "Scientific Reports",

issn = "2045-2322",

publisher = "Nature Research",

number = "1",

}

Ptacnik, R, Gomes, A, Royer, S-J, Berger, SA, Calbet, A, Nejstgaard, JC, Gasol, JM, Isari, S, Moorthi, SD, Ptacnikova, R, Striebel, M, Sazhin, AF, Tsagaraki, TM, Zervoudaki, S, Altoja, K, Dimitriou, PD, Laas, P, Gazihan, A, Martínez, RA, Schabhüttl, S, Santi, I, Sousoni, D & Pitta, P 2016, 'A light-induced shortcut in the planktonic microbial loop', Scientific Reports, vol. 6, no. 1. https://doi.org/10.1038/srep29286

TY - JOUR

T1 - A light-induced shortcut in the planktonic microbial loop

AU - Ptacnik, Robert

AU - Gomes, Ana

AU - Royer, Sarah-Jeanne

AU - Berger, Stella A.

AU - Calbet, Albert

AU - Nejstgaard, Jens C.

AU - Gasol, Josep M.

AU - Isari, Stamatina

AU - Moorthi, Stefanie D.

AU - Ptacnikova, Radka

AU - Striebel, Maren

AU - Sazhin, Andrey F.

AU - Tsagaraki, Tatiana M.

AU - Zervoudaki, Soultana

AU - Altoja, Kristi

AU - Dimitriou, Panagiotis D.

AU - Laas, Peeter

AU - Gazihan, Ayse

AU - Martínez, Rodrigo A.

AU - Schabhüttl, Stefanie

AU - Santi, Ioulia

AU - Sousoni, Despoina

AU - Pitta, Paraskevi

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: The experiment was financed by the European Union Seventh Framework Program MESOAQUA (FP7/2009–2013) coordinated by JCN under grant agreement no. 228224. MESOAQUA granted Transnational Access to R. & R.P., S.D.M., M.S., S.S., A.G., K.A., P.L. (LightDynaMix), A.C., R.A.M., A.S., A.G., S.J.R., J.M.G. (LiMic) and S.I., S.Z. (LightCopFed). R.P. further acknowledges financial support by the German Research Council (DFG Pt 5/3-1), JMG by Spanish project REMEI (CTM2015-70340) and AC by project PROTOS (CTM2009-08783) from the Spanish Ministry of Economy and Competitiveness. T. Tanaka is highly acknowledged for contributing his data on phosphorus uptake and bacterial activity. The authors wish to thank Dr. P. Divanach for valuable advice on technical matters, G. Piperakis for his inspired technical assistance throughout the experiment, S. Zivanovic and E. Dafnomili for assistance with chemical analyses, D. Podaras for assistance during the experiment and N. Sekeris for his help with constructions and ideas. The captain and the crew of the R/V Philia are also thanked for their assistance during the transportation of water from the sea to the mesocosms. Comments by three anonymous reviewers have helped improving the manuscript.

PY - 2016/7/11

Y1 - 2016/7/11

N2 - Mixotrophs combine photosynthesis with phagotrophy to cover their demands in energy and essential nutrients. This gives them a competitive advantage under oligotropihc conditions, where nutrients and bacteria concentrations are low. As the advantage for the mixotroph depends on light, the competition between mixo- and heterotrophic bacterivores should be regulated by light. To test this hypothesis, we incubated natural plankton from the ultra-oligotrophic Eastern Mediterranean in a set of mesocosms maintained at 4 light levels spanning a 10-fold light gradient. Picoplankton (heterotrophic bacteria (HB), pico-sized cyanobacteria, and small-sized flagellates) showed the fastest and most marked response to light, with pronounced predator-prey cycles, in the high-light treatments. Albeit cell specific activity of heterotrophic bacteria was constant across the light gradient, bacterial abundances exhibited an inverse relationship with light. This pattern was explained by light-induced top-down control of HB by bacterivorous phototrophic eukaryotes (PE), which was evidenced by a significant inverse relationship between HB net growth rate and PE abundances. Our results show that light mediates the impact of mixotrophic bacterivores. As mixo- and heterotrophs differ in the way they remineralize nutrients, these results have far-reaching implications for how nutrient cycling is affected by light.

AB - Mixotrophs combine photosynthesis with phagotrophy to cover their demands in energy and essential nutrients. This gives them a competitive advantage under oligotropihc conditions, where nutrients and bacteria concentrations are low. As the advantage for the mixotroph depends on light, the competition between mixo- and heterotrophic bacterivores should be regulated by light. To test this hypothesis, we incubated natural plankton from the ultra-oligotrophic Eastern Mediterranean in a set of mesocosms maintained at 4 light levels spanning a 10-fold light gradient. Picoplankton (heterotrophic bacteria (HB), pico-sized cyanobacteria, and small-sized flagellates) showed the fastest and most marked response to light, with pronounced predator-prey cycles, in the high-light treatments. Albeit cell specific activity of heterotrophic bacteria was constant across the light gradient, bacterial abundances exhibited an inverse relationship with light. This pattern was explained by light-induced top-down control of HB by bacterivorous phototrophic eukaryotes (PE), which was evidenced by a significant inverse relationship between HB net growth rate and PE abundances. Our results show that light mediates the impact of mixotrophic bacterivores. As mixo- and heterotrophs differ in the way they remineralize nutrients, these results have far-reaching implications for how nutrient cycling is affected by light.

UR - http://hdl.handle.net/10754/617092

UR - http://www.nature.com/articles/srep29286

UR - http://www.scopus.com/inward/record.url?scp=84978372549&partnerID=8YFLogxK

U2 - 10.1038/srep29286

DO - 10.1038/srep29286

M3 - Article

C2 - 27404551

SN - 2045-2322

VL - 6

JO - Scientific Reports

JF - Scientific Reports

IS - 1

ER -

A light-induced shortcut in the planktonic microbial loop

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