Seaweed for sceptics (I): a rough origin for the red algae

Artistic display of red algae
One of Ernst Haeckel’s immortal plates, a brilliant display of the diversty of forms within the red algae. Image taken from here.

 

Seaweeds are one of those things we might take for granted. Even many biologists would call this fleshy marine algae “dull” or “uninteresting” (we guess they’d be called seaweed sceptics?). One of the points of this blog is to show that life’s magnificence is to be found everywhere, if you are open to it. The thing is seaweeds are fascinating. Some of them manufacture lignin to cope with the tides. Others manufacture sulphuric acid to fend off predators. The ancestors of some seaweed can handle a pH of 0.5. It is clear that the time has come for an E&B series.

This series on seaweeds is meant to be about 3-4 posts long, interspersed with posts of unrelated content. We hope no one will remain sceptic about the fascinating nature of seaweeds after reading through the series. This initial post will deal with the evolution of the red algae, focusing on the origin of the group.

 

In the beginning there was acid (and little competition)

 

The red algae (Rhodophyta) are one of the major lineages of eukaryotic algae, with a current diversity of more than 6,000 species. Their sizes range from unicellular microscopic forms to large fleshy organisms. The vast majority of the rhodophytes inhabit marine environments (98%), where they are a key component of the algal benthos. They are especially abundant in temperate and tropical seas. A minority live in freshwater ecosystems, and even less of them thrive in acidic hot springs.

This minor minority of acidic fellows are the Cyanidiales (the only order of the class Cyanidiophyceae), unicellular red algae that live in extreme environments. They are considered the most basal group within the red algae (which is itself a fairly basal group, more on this below). The current diversity of the Cyanidiales is not yet fully assessed, with three recognized genera (Cyanidium sp., Cyanidioschyzon sp. and Galderia sp.), and a wealth of uncatalogued biodiversity according to molecular studies. The Cyanidiales are found in geothermal areas with pH values ranging from 0.2 to 4, and water temperatures up to 56ºC (the upper-temperature limit for eukaryotic phototrophs).

Cyanidium caldarium, enjoying a cheerful existence at Yellowstone National Park (Wyoming, USA). Image taken from here.

In fact, the Cyanidiales are the only phototrophs known to inhabit this hellish combination of high acidity and high temperature. Although they belong to the red algae, they lack the pigment that makes this algae red (i.e. phycoerythrin). Because of that, the Cyanidiales are greenish in colour.

The fact that the most basal members of the red algae endure acidic conditions supports the hypothesis that the first rhodophytes evolved in acidic waters, with a pH below 5. This would have been an empty ecological niche at the time, since the only other algae present were cyanobacteria (these prokaryotes do not occur in ecological niches below a pH of 5). Although cyanobacteria fare poorly in acidic environments compared to the red algae, they can thrive at higher temperatures (a high-temperature strain of Synechococcus sp. reaches 70-74 ºC).

How can it be that cyanobacteria were the only contemporary competitors of the first rhodophytes? What about all the other algae? The red algae were one of the first algal lineages to evolve and diversify (together with the Glaucophyta and the green algae, sometimes collectively called the Archaeplastida). Since the origin of the red algae virtually coincides with the origin of the eukaryotic algae as a whole, the only similar organisms present at the inception of the rhodophytes were cyanobacteria. All the other algae didn’t exist yet (as the below phylogeny aptly shows).

Evolutionary history of plastids
The evolutionary history of plastids. The red algae were amongst the first algae to evolve (through primary endosymbiosis). Also, the rhodophytes represent the origin point of a vast diversification of eukaryotic phototrophs (through secondary endosysmbiosis). Image taken from Keeling (2004).

Even though a world with almost no algae sounds alien, such was the situation 1.400 million years ago. According to molecular data, the first red algae diverged from the other eukaryotes around 1.400 million years ago. The Cyanidiales followed shortly after (they separated from the rest of the rhodophytes around 1.370 million years ago).

 

The genomic perspective

 

The first algal genomes to be fully sequenced were those of the Cyanidiales. The nuclear genome was found to be compact, with closely-spaced genes. The transposable elements represent only 0.7% of the genome, and only 0.5% of the genes have introns (a extremely low value when compared to other genomes). The number of redundant gene copies is also very low. This remarkable set of genomic features were interpreted as adaptations to the extreme environments that the Cyanidiales inhabit.

Outside of the Cyanidiales, the majority of the Rhodophyta possess multicellular fleshy thalli. The analysis of the nuclear genome of some this red seaweed revealed a set of genomic traits shared with the Cyanidiales: a small, compact genome with a low number of introns and redundant genes.

To fully grasp the genomic smallness of the red algae some comparison is needed (refer to the graph below). To put just one example, the red alga Chondrus crispus produces a multicellular structure with just 9,606 genes, far less that those present in the single-celled green alga Chlamydomonas reinheardtii (14,516 genes).

Genome graph
The structural complexity of the rhodophytes shows a striking contrast with their impoverished genome. Information on gene number from Lopez-Bautista (2010) and Collén et al. (2013). From left to right, images taken from here, here, here, here, here and here.

It’s reasonable to argue that all of the red algae share a limited gene inventory (sequenced genomes encode 5,000-10,000 genes). This indicates that the first rhodophytes went through a severe evolutionary bottleneck: a reduction of the population and the genome, with a number of introns and genes being purged.

An acidic origin for the rhodophytes is consistent with this supposed bottleneck: an extreme environment (acidic conditions coupled with high temperature) could be responsible for the strong slective pressure towards a reduce genome. Although it’s not obvious why such conditions would lead a reduced genome size, it is known that they favour small genomes in the Cyanidiales.

As a result of the genomic shrinking, a number of cellular traits were lost or greatly compromised. Flagella and centrioles are completely absent from the red algae. The loss of this beating tails means that the male gametes are unable to swim towards the female ones, complicating the fusion of gametes. Therefore, reproductive success is mainly dependant on currents, waves and chance.

The red algae are not only impaired in terms of motility and sexual reproduction. They are also impaired in terms of light perception (the lack phytochromes, light-sensing proteins). The two processes are related, sinec motility is quite pointless if you have no understanding of your surroundings. Unlike the other algae, rhodophytes don’t swim towards the light, because the can’t neither move nor see. Other losses include highly-conserved pathways for signa transduction (GPI-anchor biosynthesis) and protein degradation (autophagy).

It’s not all doom-and-gloom for the red algae. After the genomic reduction, the rhodophytes managed to escape their confinement, and invaded the seas to become a highly successful group of marine seaweed.

How did they manage to overcome such an impoverished legacy (at least in genetic terms)? Research suggests that the answer involved the recruitment of hundreds of bacterial genes via horizontal gene transfer (HGT). These bacterial genes replaced their eukaryote counterparts, and thus compensated partially for the reduced gene inventory.

 

So, to summarize…

 

The ancestors of the red algae lineage evolved into an acidic environment to avoid competition, and thus experienced a strong selective pressure to strip down the genome to its essentials. As a result, red algae were greatly impaired in  motility, sexual reproduction, light perception, intracellular signal transduction and protein degradation.

In spite of that, they managed to colonize the seas, with some help from bacteria. The rhodophytes diversified into a successful lineage, with complex multicellular thalli and even more complex sexual cycles.

 

Do we live in a green and/or red planet?

 

The red algae were critically handicapped in one respect: the possibility to “conquer” the terrestrial ecosystem. The origin of the red algae coincides with the oirigin of the eukaryotic algae, the other groups beign the glaucophytes and the green algae. Three competitors on equal foot, yet only the green algae ventured into the continent (ultimately giving rise to the land plants). The rhodophytes remained in the sea because they lack the genetic resources to face the hurdles of a terrestrial lifestyle. We don’t know about the glaucophytes (well, if someone knows, leave a comment!).

We live in a green planet, instead of a red one, thanks to an ancient bottleneck that critically impaired the red algae.

Right…?

Wrong! We live in a green and red planet. The land is undobutly green… but what about the sea? The sea is mostly red.  Through secondary endosymbiosis the rhodophytes gave rise to cryptomonads, haptophytes, heterokonts (diatoms, brown algae…) and dinoflagellates (check the gorgeous phylogeny at the beginning). A number of these lineages play vital roles in the marine ecosystem, and are extremely abundant in terms of species and individuals. In stark contrast, the green algae gave rise to the euglenids and chlorachinophytes.

A poor genetic inventory didn’t prevent the red algae from becoming a succesful lineage of seaweed. And it didn’t prevent them from fuelling a major diversification of eukaryote phototrophs either. The bulk of the marine algae can trace back their origin to a red algae. Without this peculiar group of seaweeds, the seas would be less colourful, and our world, less abundant.

 

References

Castenholz, R.W. & McDermott, T.R., 2010. The Cyanidiales: Ecology, Biodiversity, and Biogeography. In J. Seckbach & D. J. Chapman, eds. Red Algae in the Genomic Age. Dordrecht: Springer Netherlands, pp. 357–371.

Collén, J. et al., 2013. Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proceedings of the National Academy of Sciences of the United States of America, 110(13), pp.5247–52.

Collén, J., 2015. Win some, lose some: genome evolution in red algae. Journal of Phycology, 51(4), pp.621–623.

Keeling, P.J., 2004. Diversity and Evolutionary History of Plastids and Their Hosts the Tree of Eukaryotes. American Journal of Botany, 91(10), pp.1481–1493.

Lee, R.E., 2008. Phycology 4th ed., Cambridge University Press.

Lopez-Bautista, J.M., 2010. Red Algal Genomics: A Synopsis. In J. Seckbach & D. J. Chapman, eds. Red Algae in the Genomic Age. Dordrecht: Springer Netherlands, pp. 227–240.

Madigan, M.T. et al., 2012. Brock Biology of Microorganisms 13th ed., San Francisco: Benajimn Cummings.

Palmer, J.D., Soltis, D.E. & Chase, M.W., 2004. The plant tree of life: an overview and some points of view. American Journal of Botany, 91(10), pp.1437–45.

Qiu, H. et al., 2015. Evidence of ancient genome reduction in red algae (Rhodophyta) K. Valentin, ed. Journal of Phycology, 51(4), pp.624–636.

Yoon, H.S., Zuccarello, G.C. & Bhattacharya, D., 2010. Evolutionary history and taxonomy of red algae. In J. Seckbach & D. J. Chapman, eds. Red Algae in the Genomic Age. Dordrecht: Springer Netherlands, pp. 45–60.

http://blogs.scientificamerican.com/artful-amoeba/why-red-algae-never-packed-their-bags-for-land/ (last check: 26/11/1015)

http://deenr.rutgers.edu/Huan_Qiu_red_algae.html (last check: 26/11/2015)

3 Comments Add yours

  1. Were the Rhodophytes easier to tame by other eukaryotes owing to their reduced genomes? Perhaps? Any info or ideas?

    Like

    1. Staff says:

      Hi Jose, thank you for you comment. What an interesting question! I really don’t know… The reduced nuclear genome of rhodophytes perhaps could mean a “reduced identity”, that makes it easier to be assimilated. But I’ve gone through Keeling (2004) Am J Bot 91, and apparently the nucleus of the primary alga is highly reduced or lost altogehter upon secondary endosymbiosis. So I don’t know if a reduced nuclear genome makes it easier to tame a cell into a plastid. Moreover, evidence suggests red algae have been involved in secondary endosymbiosis less often than green algae. Keeling (2004) also says that plastid genomes of red algae encode more genes than plastid genomes of green algae, and that authors have suggested a greater number of genes makes it easier to acclimate to a new host.
      I am no expert on algae or plastids, from what I gather from the Keeling (2004) review, I am not sure that a reduced nuclear genomes makes it easier to be tamed into a plastid, but sure is an interesting hypothesis worth looking into!

      Like

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