Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation

Markus Lommer; Michael Specht; Alexandra Sophie Roy; Lars Kraemer; Reidar Andreson; Magdalena A. Gutowska; Juliane Wolf; Sonja V. Bergner; Markus B. Schilhabel; Ulrich C. Klostermeier; Robert G. Beiko; Philip Rosenstiel; Michael Hippler; Julie LaRoche

doi:10.1186/gb-2012-13-7-r66

Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation

Markus Lommer, Michael Specht, Alexandra Sophie Roy, Lars Kraemer, Reidar Andreson, Magdalena A. Gutowska, Juliane Wolf, Sonja V. Bergner, Markus B. Schilhabel, Ulrich C. Klostermeier, Robert G. Beiko, Philip Rosenstiel, Michael Hippler, Julie LaRoche

Résultat de recherche: Article › examen par les pairs

204 Citations (Scopus)

Résumé

Background: Biogeochemical elemental cycling is driven by primary production of biomass via phototrophic phytoplankton growth, with 40% of marine productivity being assigned to diatoms. Phytoplankton growth is widely limited by the availability of iron, an essential component of the photosynthetic apparatus. The oceanic diatom Thalassiosira oceanica shows a remarkable tolerance to low-iron conditions and was chosen as a model for deciphering the cellular response upon shortage of this essential micronutrient.Results: The combined efforts in genomics, transcriptomics and proteomics reveal an unexpected metabolic flexibility in response to iron availability for T. oceanica CCMP1005. The complex response comprises cellular retrenchment as well as remodeling of bioenergetic pathways, where the abundance of iron-rich photosynthetic proteins is lowered, whereas iron-rich mitochondrial proteins are preserved. As a consequence of iron deprivation, the photosynthetic machinery undergoes a remodeling to adjust the light energy utilization with the overall decrease in photosynthetic electron transfer complexes.Conclusions: Beneficial adaptations to low-iron environments include strategies to lower the cellular iron requirements and to enhance iron uptake. A novel contribution enhancing iron economy of phototrophic growth is observed with the iron-regulated substitution of three metal-containing fructose-bisphosphate aldolases involved in metabolic conversion of carbohydrates for enzymes that do not contain metals. Further, our data identify candidate components of a high-affinity iron-uptake system, with several of the involved genes and domains originating from duplication events. A high genomic plasticity, as seen from the fraction of genes acquired through horizontal gene transfer, provides the platform for these complex adaptations to a low-iron world.

Langue d'origine	English
Numéro d'article	R66
Journal	Genome Biology
Volume	13
Numéro de publication	7
DOI	https://doi.org/10.1186/gb-2012-13-7-r66
Statut de publication	Published - juill. 26 2012

Note bibliographique

Funding Information:
We thank Prof. Stefan Rose-John (Institute of Biochemistry, Christian-Albrechts-University Kiel, Kiel, Germany) for advice in the isolation of nuclear genomic DNA from T. oceanica and access to his laboratory and equipment, and Prof. Stefan Schreiber (Institute of Clinical Molecular Biology, Christian-Albrechts-University Kiel, Kiel, Germany) for extensive help in building up sequencing resources in Kiel. Prof. Thomas Bosch (Institute of Zoology, Christian-Albrechts-University Kiel, Kiel, Germany) and Dr Georg Hemmrich-Stanisak (Institute of Clinical Molecular Biology, Christian-Albrechts-University Kiel, Kiel, Germany) provided help with the initial contig assembly. We thank Tania Klüver (Leibniz Institute of Marine Sciences at Kiel University IFM-GEOMAR, Kiel, Germany) for help with the laboratory experiments and culturing of the algae. Dr Dhwani Desai (Leibniz Institute of Marine Sciences at Kiel University IFM-GEOMAR, Kiel, Germany) helped with bioinformatics analyses and setup of the genome browser. The upper left light micrograph in Figure 1 showing T. oceanica in valve view is courtesy of CCMP. Sequence data from F. cylindrus were produced by the US Department of Energy Joint Genome Institute [63] in collaboration with the user community. This work was supported in part by a DFG grant to JLR (RO2138/6-1) and by funding from the DFG Cluster of Excellence ‘Future Ocean’ (EXC 80) to JLR and PR. MH and JLR acknowledge funding from the BMBF ‘BIOACID’ (03F0608N) program. RA received funding from EC FP7/2007-2011 under grant agreement number PITN-GA-2008-215157 and EC FP7 Grant #205419 (ECOGENE).

ASJC Scopus Subject Areas

Ecology, Evolution, Behavior and Systematics
Genetics
Cell Biology

PubMed: MeSH publication types

Journal Article
Research Support, Non-U.S. Gov't

ODD de l’ONU

Cette action contribue à la réalisation des objectifs de développement durable suivants

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10.1186/gb-2012-13-7-r66

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Lommer, M., Specht, M., Roy, A. S., Kraemer, L., Andreson, R., Gutowska, M. A., Wolf, J., Bergner, S. V., Schilhabel, M. B., Klostermeier, U. C., Beiko, R. G., Rosenstiel, P., Hippler, M., & LaRoche, J. (2012). Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation. Genome Biology, 13(7), Article R66. https://doi.org/10.1186/gb-2012-13-7-r66

@article{458246c0c06b4063aecab365090a53ab,

title = "Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation",

abstract = "Background: Biogeochemical elemental cycling is driven by primary production of biomass via phototrophic phytoplankton growth, with 40% of marine productivity being assigned to diatoms. Phytoplankton growth is widely limited by the availability of iron, an essential component of the photosynthetic apparatus. The oceanic diatom Thalassiosira oceanica shows a remarkable tolerance to low-iron conditions and was chosen as a model for deciphering the cellular response upon shortage of this essential micronutrient.Results: The combined efforts in genomics, transcriptomics and proteomics reveal an unexpected metabolic flexibility in response to iron availability for T. oceanica CCMP1005. The complex response comprises cellular retrenchment as well as remodeling of bioenergetic pathways, where the abundance of iron-rich photosynthetic proteins is lowered, whereas iron-rich mitochondrial proteins are preserved. As a consequence of iron deprivation, the photosynthetic machinery undergoes a remodeling to adjust the light energy utilization with the overall decrease in photosynthetic electron transfer complexes.Conclusions: Beneficial adaptations to low-iron environments include strategies to lower the cellular iron requirements and to enhance iron uptake. A novel contribution enhancing iron economy of phototrophic growth is observed with the iron-regulated substitution of three metal-containing fructose-bisphosphate aldolases involved in metabolic conversion of carbohydrates for enzymes that do not contain metals. Further, our data identify candidate components of a high-affinity iron-uptake system, with several of the involved genes and domains originating from duplication events. A high genomic plasticity, as seen from the fraction of genes acquired through horizontal gene transfer, provides the platform for these complex adaptations to a low-iron world.",

author = "Markus Lommer and Michael Specht and Roy, {Alexandra Sophie} and Lars Kraemer and Reidar Andreson and Gutowska, {Magdalena A.} and Juliane Wolf and Bergner, {Sonja V.} and Schilhabel, {Markus B.} and Klostermeier, {Ulrich C.} and Beiko, {Robert G.} and Philip Rosenstiel and Michael Hippler and Julie LaRoche",

note = "Funding Information: We thank Prof. Stefan Rose-John (Institute of Biochemistry, Christian-Albrechts-University Kiel, Kiel, Germany) for advice in the isolation of nuclear genomic DNA from T. oceanica and access to his laboratory and equipment, and Prof. Stefan Schreiber (Institute of Clinical Molecular Biology, Christian-Albrechts-University Kiel, Kiel, Germany) for extensive help in building up sequencing resources in Kiel. Prof. Thomas Bosch (Institute of Zoology, Christian-Albrechts-University Kiel, Kiel, Germany) and Dr Georg Hemmrich-Stanisak (Institute of Clinical Molecular Biology, Christian-Albrechts-University Kiel, Kiel, Germany) provided help with the initial contig assembly. We thank Tania Kl{\"u}ver (Leibniz Institute of Marine Sciences at Kiel University IFM-GEOMAR, Kiel, Germany) for help with the laboratory experiments and culturing of the algae. Dr Dhwani Desai (Leibniz Institute of Marine Sciences at Kiel University IFM-GEOMAR, Kiel, Germany) helped with bioinformatics analyses and setup of the genome browser. The upper left light micrograph in Figure 1 showing T. oceanica in valve view is courtesy of CCMP. Sequence data from F. cylindrus were produced by the US Department of Energy Joint Genome Institute [63] in collaboration with the user community. This work was supported in part by a DFG grant to JLR (RO2138/6-1) and by funding from the DFG Cluster of Excellence {\textquoteleft}Future Ocean{\textquoteright} (EXC 80) to JLR and PR. MH and JLR acknowledge funding from the BMBF {\textquoteleft}BIOACID{\textquoteright} (03F0608N) program. RA received funding from EC FP7/2007-2011 under grant agreement number PITN-GA-2008-215157 and EC FP7 Grant #205419 (ECOGENE).",

year = "2012",

month = jul,

day = "26",

doi = "10.1186/gb-2012-13-7-r66",

language = "English",

volume = "13",

journal = "Genome Biology",

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TY - JOUR

T1 - Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation

AU - Lommer, Markus

AU - Specht, Michael

AU - Roy, Alexandra Sophie

AU - Kraemer, Lars

AU - Andreson, Reidar

AU - Gutowska, Magdalena A.

AU - Wolf, Juliane

AU - Bergner, Sonja V.

AU - Schilhabel, Markus B.

AU - Klostermeier, Ulrich C.

AU - Beiko, Robert G.

AU - Rosenstiel, Philip

AU - Hippler, Michael

AU - LaRoche, Julie

N1 - Funding Information: We thank Prof. Stefan Rose-John (Institute of Biochemistry, Christian-Albrechts-University Kiel, Kiel, Germany) for advice in the isolation of nuclear genomic DNA from T. oceanica and access to his laboratory and equipment, and Prof. Stefan Schreiber (Institute of Clinical Molecular Biology, Christian-Albrechts-University Kiel, Kiel, Germany) for extensive help in building up sequencing resources in Kiel. Prof. Thomas Bosch (Institute of Zoology, Christian-Albrechts-University Kiel, Kiel, Germany) and Dr Georg Hemmrich-Stanisak (Institute of Clinical Molecular Biology, Christian-Albrechts-University Kiel, Kiel, Germany) provided help with the initial contig assembly. We thank Tania Klüver (Leibniz Institute of Marine Sciences at Kiel University IFM-GEOMAR, Kiel, Germany) for help with the laboratory experiments and culturing of the algae. Dr Dhwani Desai (Leibniz Institute of Marine Sciences at Kiel University IFM-GEOMAR, Kiel, Germany) helped with bioinformatics analyses and setup of the genome browser. The upper left light micrograph in Figure 1 showing T. oceanica in valve view is courtesy of CCMP. Sequence data from F. cylindrus were produced by the US Department of Energy Joint Genome Institute [63] in collaboration with the user community. This work was supported in part by a DFG grant to JLR (RO2138/6-1) and by funding from the DFG Cluster of Excellence ‘Future Ocean’ (EXC 80) to JLR and PR. MH and JLR acknowledge funding from the BMBF ‘BIOACID’ (03F0608N) program. RA received funding from EC FP7/2007-2011 under grant agreement number PITN-GA-2008-215157 and EC FP7 Grant #205419 (ECOGENE).

PY - 2012/7/26

Y1 - 2012/7/26

N2 - Background: Biogeochemical elemental cycling is driven by primary production of biomass via phototrophic phytoplankton growth, with 40% of marine productivity being assigned to diatoms. Phytoplankton growth is widely limited by the availability of iron, an essential component of the photosynthetic apparatus. The oceanic diatom Thalassiosira oceanica shows a remarkable tolerance to low-iron conditions and was chosen as a model for deciphering the cellular response upon shortage of this essential micronutrient.Results: The combined efforts in genomics, transcriptomics and proteomics reveal an unexpected metabolic flexibility in response to iron availability for T. oceanica CCMP1005. The complex response comprises cellular retrenchment as well as remodeling of bioenergetic pathways, where the abundance of iron-rich photosynthetic proteins is lowered, whereas iron-rich mitochondrial proteins are preserved. As a consequence of iron deprivation, the photosynthetic machinery undergoes a remodeling to adjust the light energy utilization with the overall decrease in photosynthetic electron transfer complexes.Conclusions: Beneficial adaptations to low-iron environments include strategies to lower the cellular iron requirements and to enhance iron uptake. A novel contribution enhancing iron economy of phototrophic growth is observed with the iron-regulated substitution of three metal-containing fructose-bisphosphate aldolases involved in metabolic conversion of carbohydrates for enzymes that do not contain metals. Further, our data identify candidate components of a high-affinity iron-uptake system, with several of the involved genes and domains originating from duplication events. A high genomic plasticity, as seen from the fraction of genes acquired through horizontal gene transfer, provides the platform for these complex adaptations to a low-iron world.

AB - Background: Biogeochemical elemental cycling is driven by primary production of biomass via phototrophic phytoplankton growth, with 40% of marine productivity being assigned to diatoms. Phytoplankton growth is widely limited by the availability of iron, an essential component of the photosynthetic apparatus. The oceanic diatom Thalassiosira oceanica shows a remarkable tolerance to low-iron conditions and was chosen as a model for deciphering the cellular response upon shortage of this essential micronutrient.Results: The combined efforts in genomics, transcriptomics and proteomics reveal an unexpected metabolic flexibility in response to iron availability for T. oceanica CCMP1005. The complex response comprises cellular retrenchment as well as remodeling of bioenergetic pathways, where the abundance of iron-rich photosynthetic proteins is lowered, whereas iron-rich mitochondrial proteins are preserved. As a consequence of iron deprivation, the photosynthetic machinery undergoes a remodeling to adjust the light energy utilization with the overall decrease in photosynthetic electron transfer complexes.Conclusions: Beneficial adaptations to low-iron environments include strategies to lower the cellular iron requirements and to enhance iron uptake. A novel contribution enhancing iron economy of phototrophic growth is observed with the iron-regulated substitution of three metal-containing fructose-bisphosphate aldolases involved in metabolic conversion of carbohydrates for enzymes that do not contain metals. Further, our data identify candidate components of a high-affinity iron-uptake system, with several of the involved genes and domains originating from duplication events. A high genomic plasticity, as seen from the fraction of genes acquired through horizontal gene transfer, provides the platform for these complex adaptations to a low-iron world.

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SN - 1474-7596

VL - 13

JO - Genome Biology

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ER -

Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation

Résumé

Note bibliographique

ASJC Scopus Subject Areas

PubMed: MeSH publication types

ODD de l’ONU

Accès au document

Autres fichiers et liens

Empreinte numérique

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