.2021 Nov 24;288(1963):20212168.

doi: 10.1098/rspb.2021.2168. Epub 2021 Nov 24.

Unexpected cryptic species among streptophyte algae most distant to land plants

Iker Irisarri^{1 2}, Tatyana Darienko^{1 3}, Thomas Pröschold⁴, Janine M R Fürst-Jansen¹, Mahwash Jamy⁵, Jan de Vries^{1 2 6}

Affiliations

¹ Department of Applied Bioinformatics, Institute for Microbiology and Genetics, University of Goettingen, Goldschmidstrasse 1, 37077 Göttingen, Germany.
² Campus Institute Data Science (CIDAS), University of Goettingen, Goldschmidstrasse 1, 37077 Göttingen, Germany.
³ Albrecht-von-Haller-Institute of Plant Sciences, Experimental Phycology and Culture Collection of Algae, University of Goettingen, Nikolausberger Weg 18, 37073 Göttingen, Germany.
⁴ Research Department for Limnology, Leopold-Franzens-University of Innsbruck, Mondseestrasse 9, 5310 Mondsee, Austria.
⁵ Department of Organismal Biology, Program in Systematic Biology, Uppsala University, Norbyvägen 18D, 75236 Uppsala, Sweden.
⁶ Göttingen Center for Molecular Biosciences (GZMB), Department of Applied Bioinformatics, University of Goettingen, Goldschmidstrasse 1, 37077 Göttingen, Germany.

PMID:34814752
PMCID: PMC8611356
DOI: 10.1098/rspb.2021.2168

Unexpected cryptic species among streptophyte algae most distant to land plants

Iker Irisarri et al. Proc Biol Sci.2021.

.2021 Nov 24;288(1963):20212168.

doi: 10.1098/rspb.2021.2168. Epub 2021 Nov 24.

Authors

Iker Irisarri^{1 2}, Tatyana Darienko^{1 3}, Thomas Pröschold⁴, Janine M R Fürst-Jansen¹, Mahwash Jamy⁵, Jan de Vries^{1 2 6}

Affiliations

¹ Department of Applied Bioinformatics, Institute for Microbiology and Genetics, University of Goettingen, Goldschmidstrasse 1, 37077 Göttingen, Germany.
² Campus Institute Data Science (CIDAS), University of Goettingen, Goldschmidstrasse 1, 37077 Göttingen, Germany.
³ Albrecht-von-Haller-Institute of Plant Sciences, Experimental Phycology and Culture Collection of Algae, University of Goettingen, Nikolausberger Weg 18, 37073 Göttingen, Germany.
⁴ Research Department for Limnology, Leopold-Franzens-University of Innsbruck, Mondseestrasse 9, 5310 Mondsee, Austria.
⁵ Department of Organismal Biology, Program in Systematic Biology, Uppsala University, Norbyvägen 18D, 75236 Uppsala, Sweden.
⁶ Göttingen Center for Molecular Biosciences (GZMB), Department of Applied Bioinformatics, University of Goettingen, Goldschmidstrasse 1, 37077 Göttingen, Germany.

PMID:34814752
PMCID: PMC8611356
DOI: 10.1098/rspb.2021.2168

Abstract

Streptophytes are one of the major groups of the green lineage (Chloroplastida or Viridiplantae). During one billion years of evolution, streptophytes have radiated into an astounding diversity of uni- and multicellular green algae as well as land plants. Most divergent from land plants is a clade formed by Mesostigmatophyceae,Spirotaenia spp. and Chlorokybophyceae. All three lineages are species-poor and the Chlorokybophyceae consist of a single described species,Chlorokybus atmophyticus. In this study, we used phylogenomic analyses to shed light into the diversity withinChlorokybus using a sampling of isolates across its known distribution. We uncovered a consistent deep genetic structure within theChlorokybus isolates, which prompted us to formally extend the Chlorokybophyceae by describing four new species. Gene expression differences amongChlorokybus species suggest certain constitutive variability that might influence their response to environmental factors. Failure to account for this diversity can hamper comparative genomic studies aiming to understand the evolution of stress response across streptophytes. Our data highlight that future studies on the evolution of plant form and function can tap into an unknown diversity at key deep branches of the streptophytes.

Keywords: green algae; phycology; phylogenomics; plant evolution; plant terrestrialization; streptophytes.

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Figures

**Figure 1.**
Cryptic diversity inChlorokybus. (a) Maximum-likelihood phylogeny of SSU + ITS rDNA from all eleven isolates currently available in culture (rootsensufigure 3). Branch support are respectively non-parametric bootstrap proportions from neighbour-joining, maximum parsimony, maximum likelihood and Bayesian posterior probabilities and branch lengths are in expected substitutions per site. Light micrographs correspond to: (b)*C. atmophyticus* ACOI 1086, (c)*C. melkonianii* sp. nov. SAG 2609, (d)*C. bremeri* sp. nov. SAG 2611, (e)*C. riethii* sp. nov. NIES-160, (f)*C. cerffii* SAG 34.98. Scale bar = 10 µm. (Online version in colour.)

**Figure 2.**
Life cycle ofChlorokybus. (a) Zoospore with two unilaterally inserted flagella in slightly under apical position. (b) A young vegetative cell is formed after the zoospore is settled and (c) cell division can begin. (d) Two-cell stage of daughter cells are contained within the same gelatinous matrix and (e) cubic cell packages can contain groups of two to eight cells each. (f) Mature packages produce mucilage and (g) cell cycle can proceed through the production of autospores for asexual reproduction (g toe). (h) Zoospores might be formed by differentiation from autospores (g toh) or directly from mature packages (f toh). (i) Zoospores can form groups of up to 32 cells called ‘Maulbeerstadium’. Cell cycle based on Rieth [21]. (Online version in colour.)

**Figure 3.**
Transcriptomic evidence for deep phylogenetic divergences and expression differences withinChlorokybus. (a) Maximum-likelihood phylogeny based on 529 densely sampled loci, inferred with IQ-TREE under LG + F + I +Γ4 + C60 and support values from 1000 pseudoreplicates of UFBoot2 and SH-aLRT (all branches received 100% support). Branch lengths are in expected substitutions per site. (b,c) Gene expression differences (TMM, trimmed mean ofM-values) among four isolates grown simultaneously under the same experimental conditions. Heatmaps correspond to (b) the 9300 annotated proteins in theC. melkonianii genome (no filtering) and (c) the top 200 proteins with the highest expression differences. (Online version in colour.)

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References

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Unexpected cryptic species among streptophyte algae most distant to land plants

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Unexpected cryptic species among streptophyte algae most distant to land plants

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