Proteorhodophytina: Obscure Red Algae Are Keepers of Deep Evolutionary Secrets

As it turns out, I began my first postdoc just to be instantly pushed into unintended homeoffice by a global pandemic. Oh well. Why not use this time to learn more about my new subject and share what is so fascinating about it! Lets dive together into Proteorhodophytina, one of the newest recognized deep lineages of eukaryotes and a possible key to multiple mysteries of protist evolution.

Red algae (phylum Rhodophyta) are lesser known cousins of green algae and land plants (Viridiplantae) and another small algal group (Glaucophyta), which together form a vast and important eukaryotic supergroup Archaeplastida, characterized by presence of primary plastids – photosynthetic organelles of direct cyanobacterial origin.

Ernst Haeckel, Kunstformen der Natur: Florideae

Ernst Haeckel, Kunstformen der Natur: Florideae

You may be familiar with some red algae even without realizing it, as many species have profound ecological, industrial, and culinary importance! Macroscopic red algae represent one third of all seaweeds grown in aquaculture worldwide and create half of the economic value generated by this industry. Among the most commonly used are species of the genus Pyropia (formerly Porphyra; class Bangiophyceae) known as nori and used in Japanese cuisine e.g. to wrap sushi and onigiri. Chondrus crispus (class Florideophyceae) known as Irish moss is harvested for a gelatinous polysaccharide carrageenan used as a stabilizer and thickener in processed food industry, for fining beer and wine, and for traditional production of tasty milk-based desserts in Ireland or the Caribbean. Another polysaccharide of rhodophyte origin, agarose, has similar uses, but is also a ubiquitous material used in biological laboratories. Agarose is isolated from a number of red algal species of the class Florideophyceae commonly referred to as “agarophytes”.

Pyropia perforata, holdfast... (flickr.com/people/92780805@N07/)

Pyropia perforata, holdfast… (flickr.com/people/92780805@N07/)

Calcified “coralline” red algae of the class Florideophyceae which deposit calcium carbonate within their cell walls are crucial ecosystem engineers in oceans. Crustose coralline algae mechanically reinforce tropical coral reefs, reducing their erosion. Branched coralline algae provide habitat and shelter for an enormous diversity of marine animals in intertidal environments, protecting them from waves, drying, and predation. Unattached rhodolith coralline algae form extensive benthic communities, known as rhodolith beds or maërl, which are just recently being recognized as unique and important ecosystems on par with seagrass meadows or kelp forests.

On the other end of red algal diversity spectrum are extremophilic single-celled rhodophytes of the class Cyanidiophyceae which thrive in acidic and hot environments around hot springs and fumes. There are currently only three genera with eight species recognized in this class, but environmental sequencing studies hint at much greater undiscovered diversity. Phylogenetic analyses place Cyanidiophyceae as sister to all other red algae, and so their extremophilic nature was proposed to reflect the habitat of the last common ancestor of all rhodophytes. This so called “hot start” hypothesis, if true, could explain some exceptional genomic and functional simplifications observed in living red algae.

Crustose coralline algae, Peter Southwood

Crustose coralline algae, Peter Southwood

Between the large, multicellular seaweeds of Bangiophyceae and Florideophyceae classes on one hand and the extremophilic, simplified, single-celled Cyanidiophyceae on the other lie the long neglected lineages which are the true focus of this story: four classes with delightfully arcane names Rhodellophyceae, Compsopogonophyceae, Stylonematophyceae, and Porphyridiophyceae. Collectively they are known as mesophilic non-seaweed red algae and this unflattering designation easily reveals why they didn’t attract much scientific interest so far: mesophilic means they live in “normal” non-extreme conditions and non-seaweed tells that they don’t form large multicellular bodies, which would be interesting for human use or important as ecosystem creators. Members of these four classes are usually unicellular or form simple filaments, but always are tiny and inconspicuous.

It used to be assumed that mesophilic non-seaweed red algae are paraphyletic, forming several independent lineages branching one by one and representing intermediate steps between Cyanidiophyceae and the two large seaweed classes. However, recent phylogenomic analysis revealed that the four classes actually form one monophyletic lineage (sharing a single exclusive common ancestor) which was classified as a new subphylum Proteorhodophytina.

Muñoz-Gómez et al., 2017: Mesophilic Non-seaweed Red Algae Belonging to the New Subphylum Proteorhodophytina.

Muñoz-Gómez et al., 2017: Mesophilic Non-seaweed Red Algae Belonging to the New Subphylum Proteorhodophytina. (A) Bulboplastis apyrenoidosa (Rhodellophyceae) as single unicells. (B) Corynoplastis japonica (Rhodellophyceae) as a single unicell. (C) Palmelloid stage of Flintiella sanguinaria (Porphyridiophyceae). (D) Branched filaments of Rhodochaete parvula (Compsopogonophyceae). (E) Filaments of Boldia erythrosiphon (Compsopogonophyceae). (F) Filaments of Bangiopsis subsimplexm (Stylonematophyceae).

This result came as a side product of interest in another fascinating aspect of rhodophytes: their plastidal genomes. Plastids, the photosynthetic organelles of algae and plants, are in fact highly integrated bacterial symbionts and as such they usually retain remnants of their own DNA taking care of various essential functions. Plastidal genomes of red algae were generally considered to be primitive, evolutionary stable, small, efficient, and compact. They retain the highest number of genes of all studied plastids, but these genes are organized very frugally without much non-coding sequences taking up space. The structure of plastidal genomes looked very similar across the entire phylum. However, these observations were made mostly on the well-studied seaweed and extremophilic red algae, not on members of Proteorhodophytina. Sergio Muñoz-Gómez and colleagues (2017) started filling in this knowledge gap by sequencing plastidal genomes of previously neglected mesophilic non-seaweed red algae.

What they found was a very different picture. All newly sequenced plastidal genomes are larger than those of previously studied red algae and show a remarkable diversity of sizes between the various Proteorhodophytina species. One of them, Corynoplastis japonica, has the largest plastid genome which also contains the highest number of introns of all studied organisms. The Proteorhodophytina plastidal genomes are generally heavily bloated with non-coding regions and highly varied in their gene arrangement, which contrasts starkly with the conserved, compact genomes observed in seaweed and extremophilic red algae.

So far, we were discussing red algae and also touched on green algae and land plants as well as glaucophytes. All these lineages have a common origin in an ancient cell which engulfed a cyanobacterium and instead of eating it, domesticated it and learned how to use its photosynthetic machinery to make its own food from sunlight and carbon dioxide. This is the origin of the primary plastid – defining trait of the supergroup Archaeplastida. But what about other types of algae? What about kelp, forming vast, cathedral-like underwater forests? What about diatoms, living in tiny houses of glass? What about coccolithophores, whose enormous quantities form basis of chalk sediments like the white cliffs of Dover? What about dinoflagellates, which live in symbiosis with corals and whose sensitivity to climate change is causing devastating coral bleaching? There are numerous groups of algae which do not belong in Archaeplastida, and yet they also have plastids and perform photosynthesis. Most of them are so-called secondary red algae and deep origins of their plastids can be traced back to rhodophytes.

Phylogenetic Tree of Red Algal Plastid Genomes, which Resolved the Deep Phylogeny of the Phylum Rhodophyta and Established Its New Subphylum Proteorhodophytina.

Muñoz-Gómez et al., 2017: Phylogenetic Tree of Red Algal Plastid Genomes, which Resolved the Deep Phylogeny of the Phylum Rhodophyta and Established Its New Subphylum Proteorhodophytina.

In this case it was not a cyanobacterium who got eaten and tamed, but a fully developed eukaryotic cell already endowed with a well-integrated plastid. The resulting “secondary” plastids have a wide range of forms, each adapted to its new host in a different way. They usually have multiple additional membranes and some even keep a remnant nucleus of their original red algal host, creating an intricate genomic landscape in the cell. Many unanswered questions remain about these complicated plastids and their history. One of the most pressing is: How many times and in what lineages did this happen?

We are not sure whether all these lineages share a common ancestor which already had a secondary plastid (this is called “chromalveolate hypothesis”), or rather only some lineage gained the original secondary plastid, and then other, unrelated organisms have eaten and enslaved them, forming a chain of symbioses, resulting in tertiary, quaternary, or even higher degree plastids (“serial endosymbiosis”). Current understanding of the large-scale eukaryotic evolution favors the latter, more complicated scenario, but the jury is still out.

We also don’t know which lineage of red algae was the original donor of plastid. And was it only one lineage? What if there were multiple origins of secondary plastids from different branches of the rhodophyte tree of life? Phylogenetic analyses seem to endorse the notion of single origin, but the statistical support for this is low and unconvincing and such results can easily be attributed to a low number and limited diversity of red algal genomes included in the analyses. There is a lot of room for surprises. Multiple origins of secondary red plastids might actually elegantly explain certain discrepancies in previously proposed evolutionary scenarios, e.g. concerning numbers of membranes surrounding different types of secondary plastids.

Kelp Forest, NOAA

Kelp Forest, NOAA

Based on properties of secondary red plastids, we can assume that their ancestors were simple, single-celled, or colonial red algae living in moderate conditions. This description perfectly matches the newly erected subphylum Proteorhodophytina and it is possible that the ancestor (or ancestors?) of secondary red plastids was indeed member of this lineage, or closely related to it. This puts previously neglected mesophilic non-seaweed red algae in center stage of one of the greatest stories in evolutionary protistology!

In my new position in the DEEM team in Orsay, I’m joining a project which aims to gather more genomic data, both plastidal and nuclear, from a broad diversity of Proteorhodophytina and finally bring this lineage into light. We hope our results will help to answer questions about the origins of secondary plastids, as well as red algae themselves, and illuminate the differences in plastid genome architecture among them. And who knows, what other secrets we might discover in genomes of these mysterious, long-neglected creatures?

Lukas, 27/03/2020

2 thoughts on “Proteorhodophytina: Obscure Red Algae Are Keepers of Deep Evolutionary Secrets

  1. Caterina

    Very interesting and well written article. I was just looking for information about this new subphylum Proteorhodophytina ,since I’m preparing botanic exam at the university, and on internet there are very little information about this new subphylum. So thank you and I wish you all the best in your work.

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