Heterocyte glycolipids indicate polyphyly of stigonematalean cyanobacteria

Thorsten Bauersachs; Scott R. Miller; Muriel Gugger; O. Mudimu; Thomas Friedl; Lorenz Schwark

doi:10.1016/j.phytochem.2019.112059

Heterocyte glycolipids indicate polyphyly of stigonematalean cyanobacteria

Thorsten Bauersachs
, Scott R. Miller
, Muriel Gugger
, O. Mudimu
, Thomas Friedl
, Lorenz Schwark

Division of Biological and Biomedical Sciences

Kiel University
Institut Pasteur Paris
University of Göttingen
Curtin University

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

14 Scopus citations

Abstract

The cyanobacterial phylum is currently divided into five subsections (I–V), with the latter two containing no or false-branching (nostocalean) and true-branching (stigonematalean) cyanobacteria. Although morphological traits (such as cellular division and secondary branches) clearly separate both types of heterocytous cyanobacteria, molecular evidence indicates that stigonematalean cyanobacteria (Subsection V) do not form a monophyletic group but instead are interspersed and nested within the nostocalean cyanobacteria (Subsection IV). To further resolve the phylogeny of heterocytous cyanobacteria, we here analyzed the distribution of heterocyte glycolipids (HGs) in the true-branching cyanobacterium Stigonema ocellatum SAG 48.90 (type genus of Subsection V) and compared it with the HG inventory of other stigonematalean and nostocalean cyanobacteria. The most dominant HGs in S. ocellatum SAG 48.90 were 1-(O-hexose)-27-keto-3,25-octacosanediol (HG₂₈ keto-diol) and 1-(O-hexose)-3,25,27-octacosanetriol (HG₂₈ triol), which together constituted ca. 94% of all HGs. In addition, 1-(O-hexose)-3-keto-27-octacosanols (HG₂₈ keto-ols), 1-(O-hexose)-3,27-octacosanediols (HG₂₈ diols), 1-(O-hexose)-3-keto-27,29-triacontanediol (HG₃₀ keto-diol) and 1-(O-hexose)-3,27,29-triacontanetriol (HG₃₀ triol) occurred in minor abundances. Heterocyte glycolipids previously reported to be unique for stigonematalean cyanobacteria, i.e. 1-(O-hexose)-3,29,31-dotriacontanetriols (HG₃₂ triols) and 1-(O-hexose)-3-keto-29,31-dotriacontanediols (HG₃₂ keto-diols), were not detected in S. ocellatum SAG 48.90. Comparison of the HG distribution pattern with those of other heterocytous cyanobacteria indicated that S. ocellatum SAG 48.90 is most closely related to the nostocalean families Rivulariaceae and Scytonemataceae, which is complementary to reconstructed 16S rRNA gene sequence phylogenies. Our HG-based data thus provides evidence for the polyphyly of stigonematalean cyanobacteria, independent from molecular approaches, and points to the need for a critical re-evaluation of the current taxonomy of heterocytous cyanobacteria.

Original language	English
Article number	112059
Journal	Phytochemistry
Volume	166
DOIs	https://doi.org/10.1016/j.phytochem.2019.112059
State	Published - Oct 2019

Funding

Lars Wörmer is thanked for providing data on the relative abundance of HGs in the nostocalean cyanobacteria Aphanizomenon gracile UAM 521 and Calothrix sp. MU27. Nathalie Sassoon provided valuable support during the culturing of the two heterocytous cyanobacteria Calothrix sp. PCC 7103 and Scytonema sp. PCC 10023. Mareike Pohling is acknowledged for laboratory assistance during lipid extraction. Two anonymous reviewers are thanked for their constructive comments on the manuscript. SRM was supported by award NNA15BB04A from the National Aeronautics and Space Administration, US. The collection “Pasteur Culture of Cyanobacteria” is funded by the Institut Pasteur, France. Lars Wörmer is thanked for providing data on the relative abundance of HGs in the nostocalean cyanobacteria Aphanizomenon gracile UAM 521 and Calothrix sp. MU27. Nathalie Sassoon provided valuable support during the culturing of the two heterocytous cyanobacteria Calothrix sp. PCC 7103 and Scytonema sp. PCC 10023. Mareike Pohling is acknowledged for laboratory assistance during lipid extraction. Two anonymous reviewers are thanked for their constructive comments on the manuscript. SRM was supported by award NNA15BB04A from the National Aeronautics and Space Administration, US . The collection “Pasteur Culture of Cyanobacteria” is funded by the Institut Pasteur, France .

Funders	Funder number
National Aeronautics and Space Administration	NNA15BB04A
Institut Pasteur de Lille

Keywords

Calothrix sp.
Chemotaxonomy
Intact polar lipids
Mastigocladus laminosus
Nostocales
Polyphyly
Scytonema sp.
Stigonema ocellatum
Stigonematales
True-branching cyanobacteria

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10.1016/j.phytochem.2019.112059

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@article{700af507796b4bdab0ea2c543bb8bc21,

title = "Heterocyte glycolipids indicate polyphyly of stigonematalean cyanobacteria",

abstract = "The cyanobacterial phylum is currently divided into five subsections (I–V), with the latter two containing no or false-branching (nostocalean) and true-branching (stigonematalean) cyanobacteria. Although morphological traits (such as cellular division and secondary branches) clearly separate both types of heterocytous cyanobacteria, molecular evidence indicates that stigonematalean cyanobacteria (Subsection V) do not form a monophyletic group but instead are interspersed and nested within the nostocalean cyanobacteria (Subsection IV). To further resolve the phylogeny of heterocytous cyanobacteria, we here analyzed the distribution of heterocyte glycolipids (HGs) in the true-branching cyanobacterium Stigonema ocellatum SAG 48.90 (type genus of Subsection V) and compared it with the HG inventory of other stigonematalean and nostocalean cyanobacteria. The most dominant HGs in S. ocellatum SAG 48.90 were 1-(O-hexose)-27-keto-3,25-octacosanediol (HG28 keto-diol) and 1-(O-hexose)-3,25,27-octacosanetriol (HG28 triol), which together constituted ca. 94\% of all HGs. In addition, 1-(O-hexose)-3-keto-27-octacosanols (HG28 keto-ols), 1-(O-hexose)-3,27-octacosanediols (HG28 diols), 1-(O-hexose)-3-keto-27,29-triacontanediol (HG30 keto-diol) and 1-(O-hexose)-3,27,29-triacontanetriol (HG30 triol) occurred in minor abundances. Heterocyte glycolipids previously reported to be unique for stigonematalean cyanobacteria, i.e. 1-(O-hexose)-3,29,31-dotriacontanetriols (HG32 triols) and 1-(O-hexose)-3-keto-29,31-dotriacontanediols (HG32 keto-diols), were not detected in S. ocellatum SAG 48.90. Comparison of the HG distribution pattern with those of other heterocytous cyanobacteria indicated that S. ocellatum SAG 48.90 is most closely related to the nostocalean families Rivulariaceae and Scytonemataceae, which is complementary to reconstructed 16S rRNA gene sequence phylogenies. Our HG-based data thus provides evidence for the polyphyly of stigonematalean cyanobacteria, independent from molecular approaches, and points to the need for a critical re-evaluation of the current taxonomy of heterocytous cyanobacteria.",

keywords = "Calothrix sp., Chemotaxonomy, Intact polar lipids, Mastigocladus laminosus, Nostocales, Polyphyly, Scytonema sp., Stigonema ocellatum, Stigonematales, True-branching cyanobacteria",

author = "Thorsten Bauersachs and Miller, \{Scott R.\} and Muriel Gugger and O. Mudimu and Thomas Friedl and Lorenz Schwark",

note = "Publisher Copyright: {\textcopyright} 2019 Elsevier Ltd",

year = "2019",

month = oct,

doi = "10.1016/j.phytochem.2019.112059",

language = "English",

volume = "166",

journal = "Phytochemistry",

issn = "0031-9422",

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TY - JOUR

T1 - Heterocyte glycolipids indicate polyphyly of stigonematalean cyanobacteria

AU - Bauersachs, Thorsten

AU - Miller, Scott R.

AU - Gugger, Muriel

AU - Mudimu, O.

AU - Friedl, Thomas

AU - Schwark, Lorenz

PY - 2019/10

Y1 - 2019/10

N2 - The cyanobacterial phylum is currently divided into five subsections (I–V), with the latter two containing no or false-branching (nostocalean) and true-branching (stigonematalean) cyanobacteria. Although morphological traits (such as cellular division and secondary branches) clearly separate both types of heterocytous cyanobacteria, molecular evidence indicates that stigonematalean cyanobacteria (Subsection V) do not form a monophyletic group but instead are interspersed and nested within the nostocalean cyanobacteria (Subsection IV). To further resolve the phylogeny of heterocytous cyanobacteria, we here analyzed the distribution of heterocyte glycolipids (HGs) in the true-branching cyanobacterium Stigonema ocellatum SAG 48.90 (type genus of Subsection V) and compared it with the HG inventory of other stigonematalean and nostocalean cyanobacteria. The most dominant HGs in S. ocellatum SAG 48.90 were 1-(O-hexose)-27-keto-3,25-octacosanediol (HG28 keto-diol) and 1-(O-hexose)-3,25,27-octacosanetriol (HG28 triol), which together constituted ca. 94% of all HGs. In addition, 1-(O-hexose)-3-keto-27-octacosanols (HG28 keto-ols), 1-(O-hexose)-3,27-octacosanediols (HG28 diols), 1-(O-hexose)-3-keto-27,29-triacontanediol (HG30 keto-diol) and 1-(O-hexose)-3,27,29-triacontanetriol (HG30 triol) occurred in minor abundances. Heterocyte glycolipids previously reported to be unique for stigonematalean cyanobacteria, i.e. 1-(O-hexose)-3,29,31-dotriacontanetriols (HG32 triols) and 1-(O-hexose)-3-keto-29,31-dotriacontanediols (HG32 keto-diols), were not detected in S. ocellatum SAG 48.90. Comparison of the HG distribution pattern with those of other heterocytous cyanobacteria indicated that S. ocellatum SAG 48.90 is most closely related to the nostocalean families Rivulariaceae and Scytonemataceae, which is complementary to reconstructed 16S rRNA gene sequence phylogenies. Our HG-based data thus provides evidence for the polyphyly of stigonematalean cyanobacteria, independent from molecular approaches, and points to the need for a critical re-evaluation of the current taxonomy of heterocytous cyanobacteria.

AB - The cyanobacterial phylum is currently divided into five subsections (I–V), with the latter two containing no or false-branching (nostocalean) and true-branching (stigonematalean) cyanobacteria. Although morphological traits (such as cellular division and secondary branches) clearly separate both types of heterocytous cyanobacteria, molecular evidence indicates that stigonematalean cyanobacteria (Subsection V) do not form a monophyletic group but instead are interspersed and nested within the nostocalean cyanobacteria (Subsection IV). To further resolve the phylogeny of heterocytous cyanobacteria, we here analyzed the distribution of heterocyte glycolipids (HGs) in the true-branching cyanobacterium Stigonema ocellatum SAG 48.90 (type genus of Subsection V) and compared it with the HG inventory of other stigonematalean and nostocalean cyanobacteria. The most dominant HGs in S. ocellatum SAG 48.90 were 1-(O-hexose)-27-keto-3,25-octacosanediol (HG28 keto-diol) and 1-(O-hexose)-3,25,27-octacosanetriol (HG28 triol), which together constituted ca. 94% of all HGs. In addition, 1-(O-hexose)-3-keto-27-octacosanols (HG28 keto-ols), 1-(O-hexose)-3,27-octacosanediols (HG28 diols), 1-(O-hexose)-3-keto-27,29-triacontanediol (HG30 keto-diol) and 1-(O-hexose)-3,27,29-triacontanetriol (HG30 triol) occurred in minor abundances. Heterocyte glycolipids previously reported to be unique for stigonematalean cyanobacteria, i.e. 1-(O-hexose)-3,29,31-dotriacontanetriols (HG32 triols) and 1-(O-hexose)-3-keto-29,31-dotriacontanediols (HG32 keto-diols), were not detected in S. ocellatum SAG 48.90. Comparison of the HG distribution pattern with those of other heterocytous cyanobacteria indicated that S. ocellatum SAG 48.90 is most closely related to the nostocalean families Rivulariaceae and Scytonemataceae, which is complementary to reconstructed 16S rRNA gene sequence phylogenies. Our HG-based data thus provides evidence for the polyphyly of stigonematalean cyanobacteria, independent from molecular approaches, and points to the need for a critical re-evaluation of the current taxonomy of heterocytous cyanobacteria.

KW - Calothrix sp.

KW - Chemotaxonomy

KW - Intact polar lipids

KW - Mastigocladus laminosus

KW - Nostocales

KW - Polyphyly

KW - Scytonema sp.

KW - Stigonema ocellatum

KW - Stigonematales

KW - True-branching cyanobacteria

UR - https://www.scopus.com/pages/publications/85068268857

U2 - 10.1016/j.phytochem.2019.112059

DO - 10.1016/j.phytochem.2019.112059

M3 - Article

C2 - 31280092

AN - SCOPUS:85068268857

SN - 0031-9422

VL - 166

JO - Phytochemistry

JF - Phytochemistry

M1 - 112059

ER -

Heterocyte glycolipids indicate polyphyly of stigonematalean cyanobacteria

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Keywords

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