Abstract

Glaucophyta are members of the Archaeplastida, the founding group of photosynthetic eukaryotes that also includes red algae (Rhodophyta), green algae, and plants (Viridiplantae). Here we present a high-quality assembly, built using long-read sequences, of the ca. 100 Mb nuclear genome of the model glaucophyte Cyanophora paradoxa. We also conducted a quick-freeze deep-etch electron microscopy (QFDEEM) analysis of C. paradoxa cells to investigate glaucophyte morphology in comparison to other organisms. Using the genome data, we generated a resolved 115-taxon eukaryotic tree of life that includes a well-supported, monophyletic Archaeplastida. Analysis of muroplast peptidoglycan (PG) ultrastructure using QFDEEM shows that PG is most dense at the cleavage-furrow. Analysis of the chlamydial contribution to glaucophytes and other Archaeplastida shows that these foreign sequences likely played a key role in anaerobic glycolysis in primordial algae to alleviate ATP starvation under night-time hypoxia. The robust genome assembly of C. paradoxa significantly advances knowledge about this model species and provides a reference for exploring the panoply of traits associated with the anciently diverged glaucophyte lineage.

Highlights

  • The glaucophyte algae (Glaucophyta1) are a small group of unicellular and colonial taxa with four described genera and about 15 species (Fig. 1)

  • We provide a detailed analysis of C. paradoxa cell ultrastructure to assess existing hypotheses about the morphological evolution of this lineage

  • The DNA was sent to the Max Planck Institute genome sequencing centre for library construction (Cologne, Germany) and six SMRT cells were sequenced on an RSII instrument using P6-C4 chemistry, producing over 7.46 Gb of long-read sequence data with an average insert size of ca. 15 kb

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Summary

Introduction

The glaucophyte algae (Glaucophyta1) are a small group of unicellular and colonial taxa with four described genera and about 15 species (Fig. 1). 1.6 billion years ago through primary endosymbiosis.[3,4,5,6] The green algae in this ‘supergroup’ gave rise to plants, and the plastids of red and green algae were spread via serial endosymbioses to a myriad of other important primary producers including diatoms, haptophytes, dinoflagellates, and euglenids.[7] What makes glaucophytes of particular interest is that they uniquely retain a suite of plastid traits associated with the ancestral cyanobacterial endosymbiont, such as peptidoglycan (PG) and phycobilisomes, and lack chlorophyll-b.8,9 This lineage harbours the primordial, bacterial (putatively chlamydial) derived UhpC-type hexose-phosphate transporter to translocate fixed carbon from the plastid to the host cytosol. These wide-ranging results paint a fascinating picture of glaucophyte evolution and identify features that both unite and distinguish C. paradoxa from its Archaeplastida sisters

Genome sequencing
Illumina RNA-Seq
Illumina genome data
Analysis of repeat content
Gene prediction
Single nucleotide polymorphism detection
Phylogenomics of individual predicted proteins
Differential gene-expression analysis
Eukaryote tree of life
Transcriptomic response to light
Insights into the ultrastructure of cyanophora paradoxa
Alveoli
Pyrenoid
Thylakoids and phycobilisomes
Peptidoglycan
Other cellular features
Evolutionary history of PG biosynthesis in glaucophytes
Analysis of chlamydial HGTs
Conclusive remarks
Full Text
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