Predominance of deterministic microbial community dynamics in salterns exposed to different light intensities

Tomeu Viver; Luis H. Orellana; Sara Díaz; Mercedes Urdiain; María Dolores Ramos-Barbero; José E. González-Pastor; Aharon Oren; Janet K. Hatt; Rudolf Amann; Josefa Antón; Konstantinos T. Konstantinidis; Ramon Rosselló-Móra

doi:10.1111/1462-2920.14790

Predominance of deterministic microbial community dynamics in salterns exposed to different light intensities

Tomeu Viver^*, Luis H. Orellana, Sara Díaz, Mercedes Urdiain, María Dolores Ramos-Barbero, José E. González-Pastor, Aharon Oren, Janet K. Hatt, Rudolf Amann, Josefa Antón, Konstantinos T. Konstantinidis, Ramon Rosselló-Móra

^*Corresponding author for this work

Department of Plant and Environmental Sciences (Natural Sciences)

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

14 Scopus citations

Abstract

While the dynamics of microbial community assembly driven by environmental perturbations have been extensively studied, our understanding is far from complete, particularly for light-induced perturbations. Extremely halophilic communities thriving in coastal solar salterns are mainly influenced by two environmental factors—salt concentrations and high sunlight irradiation. By experimentally manipulating light intensity through the application of shading, we showed that light acts as a deterministic factor that ultimately drives the establishment of recurrent microbial communities under near-saturation salt concentrations. In particular, the stable and highly change-resistant communities that established under high-light intensities were dominated (>90% of metagenomic reads) by Haloquadratum spp. and Salinibacter spp. On the other hand, under 37-fold lower light intensity, different, less stable and change-resistant communities were established, mainly dominated by yet unclassified haloarchaea and relatively diverse photosynthetic microorganisms. These communities harboured, in general, much lower carotenoid pigment content than their high-irradiation counterparts. Both assemblage types appeared to be highly resilient, re-establishing when favourable conditions returned after perturbation (i.e. high-irradiation for the former communities and low-irradiation for the latter ones). Overall, our results revealed that stochastic processes were of limited significance to explain these patterns.

Original language	American English
Pages (from-to)	4300-4315
Number of pages	16
Journal	Environmental Microbiology
Volume	21
Issue number	11
DOIs	https://doi.org/10.1111/1462-2920.14790
State	Published - 1 Nov 2019

Bibliographical note

Funding Information:
The authors would like to thank Vladimir Benes and Arantxa López for metagenomes sequencing. The authors would particularly like to thank the whole team at Salines d'esTrenc and Flor de Sal SL for allowing the access to their facilities and their support in performing the experiments. This study was funded by the Spanish Ministry of Economy projects CGL2012-39627-C03-03 CLG2015_66686-C3-1-P and PGC2018-096956-B-C41 (to R.R.M.), CGL2015_66686-C3-3-P (to J.A.) and CGL2015_66686-C3-2-P (to J.E.G.P.), which were also supported with European Regional Development Fund (FEDER) funds. R.A. was funded by the Max Planck Society. KTK's research was supported, in part, by the U.S. National Science Foundation (Award No. 1831582). T.V.P. received a pre-doctoral fellowship (No. BES-2013-064420) from the Spanish Government Ministry for Finance and Competition. R.R.M. acknowledges the financial support of the sabbatical stay at Georgia Tech supported by the Grant PRX18/00048 of the Ministry of Sciences, Innovation and Universities.

Publisher Copyright:
© 2019 Society for Applied Microbiology and John Wiley & Sons Ltd.

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10.1111/1462-2920.14790

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Viver, T., Orellana, L. H., Díaz, S., Urdiain, M., Ramos-Barbero, M. D., González-Pastor, J. E., Oren, A., Hatt, J. K., Amann, R., Antón, J., Konstantinidis, K. T., & Rosselló-Móra, R. (2019). Predominance of deterministic microbial community dynamics in salterns exposed to different light intensities. Environmental Microbiology, 21(11), 4300-4315. https://doi.org/10.1111/1462-2920.14790

@article{03ac44829cb3491fabb52e1884415d8e,

title = "Predominance of deterministic microbial community dynamics in salterns exposed to different light intensities",

abstract = "While the dynamics of microbial community assembly driven by environmental perturbations have been extensively studied, our understanding is far from complete, particularly for light-induced perturbations. Extremely halophilic communities thriving in coastal solar salterns are mainly influenced by two environmental factors—salt concentrations and high sunlight irradiation. By experimentally manipulating light intensity through the application of shading, we showed that light acts as a deterministic factor that ultimately drives the establishment of recurrent microbial communities under near-saturation salt concentrations. In particular, the stable and highly change-resistant communities that established under high-light intensities were dominated (>90% of metagenomic reads) by Haloquadratum spp. and Salinibacter spp. On the other hand, under 37-fold lower light intensity, different, less stable and change-resistant communities were established, mainly dominated by yet unclassified haloarchaea and relatively diverse photosynthetic microorganisms. These communities harboured, in general, much lower carotenoid pigment content than their high-irradiation counterparts. Both assemblage types appeared to be highly resilient, re-establishing when favourable conditions returned after perturbation (i.e. high-irradiation for the former communities and low-irradiation for the latter ones). Overall, our results revealed that stochastic processes were of limited significance to explain these patterns.",

author = "Tomeu Viver and Orellana, {Luis H.} and Sara D{\'i}az and Mercedes Urdiain and Ramos-Barbero, {Mar{\'i}a Dolores} and Gonz{\'a}lez-Pastor, {Jos{\'e} E.} and Aharon Oren and Hatt, {Janet K.} and Rudolf Amann and Josefa Ant{\'o}n and Konstantinidis, {Konstantinos T.} and Ramon Rossell{\'o}-M{\'o}ra",

note = "Funding Information: The authors would like to thank Vladimir Benes and Arantxa L{\'o}pez for metagenomes sequencing. The authors would particularly like to thank the whole team at Salines d'esTrenc and Flor de Sal SL for allowing the access to their facilities and their support in performing the experiments. This study was funded by the Spanish Ministry of Economy projects CGL2012-39627-C03-03 CLG2015_66686-C3-1-P and PGC2018-096956-B-C41 (to R.R.M.), CGL2015_66686-C3-3-P (to J.A.) and CGL2015_66686-C3-2-P (to J.E.G.P.), which were also supported with European Regional Development Fund (FEDER) funds. R.A. was funded by the Max Planck Society. KTK's research was supported, in part, by the U.S. National Science Foundation (Award No. 1831582). T.V.P. received a pre-doctoral fellowship (No. BES-2013-064420) from the Spanish Government Ministry for Finance and Competition. R.R.M. acknowledges the financial support of the sabbatical stay at Georgia Tech supported by the Grant PRX18/00048 of the Ministry of Sciences, Innovation and Universities. Publisher Copyright: {\textcopyright} 2019 Society for Applied Microbiology and John Wiley & Sons Ltd.",

year = "2019",

month = nov,

day = "1",

doi = "10.1111/1462-2920.14790",

language = "American English",

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Viver, T, Orellana, LH, Díaz, S, Urdiain, M, Ramos-Barbero, MD, González-Pastor, JE, Oren, A, Hatt, JK, Amann, R, Antón, J, Konstantinidis, KT & Rosselló-Móra, R 2019, 'Predominance of deterministic microbial community dynamics in salterns exposed to different light intensities', Environmental Microbiology, vol. 21, no. 11, pp. 4300-4315. https://doi.org/10.1111/1462-2920.14790

TY - JOUR

T1 - Predominance of deterministic microbial community dynamics in salterns exposed to different light intensities

AU - Viver, Tomeu

AU - Orellana, Luis H.

AU - Díaz, Sara

AU - Urdiain, Mercedes

AU - Ramos-Barbero, María Dolores

AU - González-Pastor, José E.

AU - Oren, Aharon

AU - Hatt, Janet K.

AU - Amann, Rudolf

AU - Antón, Josefa

AU - Konstantinidis, Konstantinos T.

AU - Rosselló-Móra, Ramon

N1 - Funding Information: The authors would like to thank Vladimir Benes and Arantxa López for metagenomes sequencing. The authors would particularly like to thank the whole team at Salines d'esTrenc and Flor de Sal SL for allowing the access to their facilities and their support in performing the experiments. This study was funded by the Spanish Ministry of Economy projects CGL2012-39627-C03-03 CLG2015_66686-C3-1-P and PGC2018-096956-B-C41 (to R.R.M.), CGL2015_66686-C3-3-P (to J.A.) and CGL2015_66686-C3-2-P (to J.E.G.P.), which were also supported with European Regional Development Fund (FEDER) funds. R.A. was funded by the Max Planck Society. KTK's research was supported, in part, by the U.S. National Science Foundation (Award No. 1831582). T.V.P. received a pre-doctoral fellowship (No. BES-2013-064420) from the Spanish Government Ministry for Finance and Competition. R.R.M. acknowledges the financial support of the sabbatical stay at Georgia Tech supported by the Grant PRX18/00048 of the Ministry of Sciences, Innovation and Universities. Publisher Copyright: © 2019 Society for Applied Microbiology and John Wiley & Sons Ltd.

PY - 2019/11/1

Y1 - 2019/11/1

N2 - While the dynamics of microbial community assembly driven by environmental perturbations have been extensively studied, our understanding is far from complete, particularly for light-induced perturbations. Extremely halophilic communities thriving in coastal solar salterns are mainly influenced by two environmental factors—salt concentrations and high sunlight irradiation. By experimentally manipulating light intensity through the application of shading, we showed that light acts as a deterministic factor that ultimately drives the establishment of recurrent microbial communities under near-saturation salt concentrations. In particular, the stable and highly change-resistant communities that established under high-light intensities were dominated (>90% of metagenomic reads) by Haloquadratum spp. and Salinibacter spp. On the other hand, under 37-fold lower light intensity, different, less stable and change-resistant communities were established, mainly dominated by yet unclassified haloarchaea and relatively diverse photosynthetic microorganisms. These communities harboured, in general, much lower carotenoid pigment content than their high-irradiation counterparts. Both assemblage types appeared to be highly resilient, re-establishing when favourable conditions returned after perturbation (i.e. high-irradiation for the former communities and low-irradiation for the latter ones). Overall, our results revealed that stochastic processes were of limited significance to explain these patterns.

AB - While the dynamics of microbial community assembly driven by environmental perturbations have been extensively studied, our understanding is far from complete, particularly for light-induced perturbations. Extremely halophilic communities thriving in coastal solar salterns are mainly influenced by two environmental factors—salt concentrations and high sunlight irradiation. By experimentally manipulating light intensity through the application of shading, we showed that light acts as a deterministic factor that ultimately drives the establishment of recurrent microbial communities under near-saturation salt concentrations. In particular, the stable and highly change-resistant communities that established under high-light intensities were dominated (>90% of metagenomic reads) by Haloquadratum spp. and Salinibacter spp. On the other hand, under 37-fold lower light intensity, different, less stable and change-resistant communities were established, mainly dominated by yet unclassified haloarchaea and relatively diverse photosynthetic microorganisms. These communities harboured, in general, much lower carotenoid pigment content than their high-irradiation counterparts. Both assemblage types appeared to be highly resilient, re-establishing when favourable conditions returned after perturbation (i.e. high-irradiation for the former communities and low-irradiation for the latter ones). Overall, our results revealed that stochastic processes were of limited significance to explain these patterns.

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U2 - 10.1111/1462-2920.14790

DO - 10.1111/1462-2920.14790

M3 - Article

C2 - 31444990

AN - SCOPUS:85074079002

SN - 1462-2912

VL - 21

SP - 4300

EP - 4315

JO - Environmental Microbiology

JF - Environmental Microbiology

IS - 11

ER -

Predominance of deterministic microbial community dynamics in salterns exposed to different light intensities

Abstract

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