The pros and cons of cell walls …

Vaucheria_x100_190630_#1

When I wrote about Vaucheria in a recent post I mentioned that it is “siphonous”, meaning that there are no cross walls dividing the filament into individual cells. Instead, the organism consists of branching tubes containing many separate nuclei and chloroplasts (see “When the going gets tough …”). What I did not do was explain why this might be of benefit to a stream-dwelling organism.

Many scientists over the years have considered the benefits that accrued when simple unicellular organisms banded together to form the first multicellular organisms. They’ve come up with a number of theories, all of which may apply in some cases. However, having accepted that multicellular organisms have a number of advantages over single cells, we have to ask why organisms such as Vaucheria seem to have gone one step further: not only have several cells banded together but they also seem to have lost the cell walls that usually separate the individual units. Most biologists, nurtured in the belief that the cell is the basic unit from which organisms are built, will find Vaucheria’s growth form to be a surprise.

The usefulness of cells, in an evolutionary context, is that this opens the way to specialisation and, over time, to the development of tissues within organisms dedicated to particular tasks. We could think of cells as tiny bags, each containing mixtures of enzymes most relevant to their function. Cells in a leaf, for example, will need to focus on producing enzymes required for photosynthesis whilst those in the trunk will be programmed to produce structural tissues. Cells, in other words, facilitate this division of labour within plants. However, a simple filamentous alga has far fewer needs than a mighty oak tree: the water around them provide both support (so complicated structural tissues are not needed) and a supply of nutrients (removing the need for internal plumbing). If there is less need for specialisation, then there is also less need to invest energy in building cell walls which, despite their advantages, also limit the capacity of cells to share resources. Cells of many algae and all higher plants have channels called “plasmadesmata” which link them together; however, these require energy to function.

If you will excuse a topical, somewhat teleological and rather tortuous metaphor, all plants have the choice of either a “trade deal” (investing energy in plasmadesmata in return for resources from neighbouring cells) or “open borders” (ditching cell walls and sharing resources). For most land plants, the former makes more sense; different lineages of algae, on the other hand, have dabbled in both strategies and Vaucheria represents a successful example of the latter. “Successful”, you sneer, “… it thrives in small clumps in polluted rivers. How is that successful?”. That, if I may say so, is a very terrestrio-centric view of the world: Vaucheria lives in a world where it does not need extensive investment in the tissues that comprise the organisms that are paraded before our eyes on the Living Planet. It has all it needs and neither boasts nor worries about tomorrow.

Vaucheria_x400_190630_#2

Siphon of Vaucheria with a side-branch, collected from the River Browney, Co. Durham and photographed at 400x magnification. Note the absence of cell walls. Scale bar: 20 micrometres (= 1/50th of a millimetre). The photograph at the top of the post shows more siphons, at 100x magnification. Scale bar: 100 micrometres (= 1/10th of a millimetre).

We can find siphonous algae not just in the Xanthophyta (the division to which Vaucheria belongs) but also in some lineages of the green algae, including the important marine genus Caulerpera. Cladophora, no stranger to these posts (see “Summertime blues …”) is siphonocladous, rather than strictly siphonous, meaning that it is divided into large cells, each of which contains many nuclei rather than the single nucleus that is characteristic of most cells throughout the plant and animal kingdoms. Balanced against this, there is a much greater number of multicellular algae that retain cell walls, some of which show considerable differentiation of tissue. Modern land plants arose from this latter largely because of the opportunities this differentiation offered. Being siphonous (or siphonocladous) has proved to be a good strategy under certain circumstances but, in turn, limits the options for the species to extend into new habitats.

In my earlier post I used the metaphor of a “sausage skin” to describe Vaucheria. Most of the interior of the organism is taken up by a vacuole, with the chloroplasts and other cell machinery pressed into a narrow band just inside the cell wall. If you watch closely, you can see the chloroplasts in living Vaucheria moving very slowly – a process called “cytoplasmic streaming”. In very bright light the chloroplasts gather at the sides, so protecting each other from harm (see “Good vibrations under the Suffolk sun …” for another way around this problem). The nuclei and mitochondria (the cell’s “batteries”) can also move around and studies have shown all three move by different mechanisms. Being a siphonous organism offers more prospects for this means of adaptation to local circumstances but, overall, the pros are outweighed by the cons, and there are far more genera of multicellular algae than there of siphonous or siphonocladous algae. Vaucheria and other siphonous algae are clearly very successful in a few habitats but the big picture suggests that being truly multicellular offered organisms far more options in the long term.

References
Coneva, V., & Chitwood, D. H. (2015). Plant architecture without multicellularity: quandaries over patterning and the soma-germline divide in siphonous algae. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2015.00287

Herron, M. D., Borin, J. M., Boswell, J. C., Walker, J., Chen, I.-C. K., Knox, C. A., … Ratcliff, W. C. (2019). De novo origins of multicellularity in response to predation. Scientific Reports. https://doi.org/10.1038/s41598-019-39558-8

Canter-Lund, H. & Lund, J.W.G. (1995). Freshwater Algae: Their Microscopic World Explored. Biopress, Bristol.

Ott, D.W. & Brown, R.M. (1974). Developmental cytology of the genus Vaucheria 1. organisation of the vegetative filament. British Phycological Journal 9: 111 – 126.

Pennisi, E. (2018). The momentous transition to multicellular life may not have been so hard after all. Science, New York. doi:10.1126/science.aau5806

Raven, J.A. (1997). Minireview: multiple origins of plasmadesmata. European Journal of Phycology 32: 95-101.

Vroom, P.S. & C.A. Smith (2001). The challenge of siphonous green algae. American Scientist 89: 525-531.

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When the going gets tough …

Castle_Eden_Dene_May19

Two months after the visit I described in the previous post I was back at Castle Eden Dene.    The trees were now in leaf and the floor of the forest was carpeted with wild garlic.   The stream, however, had disappeared below the surface and, once again, I could walk along the channel without getting my feet damp.

Having found a rich crop of diatoms on my last visit when the stream was dry I was intrigued to see what was growing on the stones this time, so I used a toothbrush and some water that I had brought along to scrub a few and collected the dislodged material in my white tray.   I was intrigued to see that the suspension that collected in my tray had a distinct green tinge and, when I got a drop of it under my microscope, found it to be dominated by small green cells.  These were superficially similar to the cells of Desmococcus and Apatococcus that I found on the fence in my garden (see “Little Round Green Things …”) but this is a difficult group with not many clear morphological features with which to distinguish genera so I sent a sample off to Dave John for his opinion.

His view is also that groups such as this are almost impossible to identify unless you grow them in the laboratory or have access to DNA sequencing facilities.   He commented that Desmococcus and Apatococcus both have distinctive 2- or 4-celled packets of cells, which were not common in the Castle Eden Dene sample.  Likely candidates are the generaPleurastrumand Pseudopleurococcus, both of which are subaerial or terrestrial.   Perhaps “Little Round Green Things” is as close as we need to go in this particular instance?

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A distinctly-green suspension of the biofilm on stones at Castle Eden Dene in May 2019 (left) along with a magnified view showing some of the green cells which dominated the sample (right).  Scale bar: 20 micrometres (1/5thof a millimetre).   

A short distance further on I found some mats of entwined filaments on the tops of stones which also piqued my curiosity.   Under the microscope, and with the addition of a drop of water to rehydrate them, these filaments revealed themselves to belong to Vaucheria (see “Who do you think you are?”).   Technically speaking, Vaucheria is not filamentous but “siphonous”, meaning that there are no cross walls but, instead, the organism consists of branching tubes containing many separate nuclei and chloroplasts.  The cell walls of Vaucheria, however, rupture easily releasing the chloroplasts and giving the appearance of an empty sausage skin. In this case, there are still quite a few chloroplasts but a healthy Vaucheria filament has a uniformly dense green appearance that none of those that I saw in Castle Eden Burn possessed.

There was more than just vegetative filaments of Vaucheria here: scattered amongst them were some larger, spheroid or jar-shaped cells, which are part of Vaucheria’s sexual reproduction apparatus.   I’ve talked before in this blog about how sexual reproduction is relatively rare in the filamentous algae that we find in lakes and streams (see “The perplexing case of the celibate alga …”) and Vaucheria is another case in point.   Put simply, many algae do not bother with sexual reproduction when conditions are favourable and they can grow through simple cell division.   If you subjected a Vaucheria filament to Freudian analysis, it would probably tell you that one outcome of sexual reproduction was a 50% dilution of its unique genotype. So why bother if you don’t have to?  On the other hand, sexual reproduction in these organisms usually results in a zygote with a thick wall that is capable of resisting tough conditions.   The complete absence of water in Castle Eden Burn would be one such circumstance.   To put it another way, when the going gets tough, the algae get frisky.

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Mats of Vaucheria growing on a small boulder in Castle Eden Dene in May 2019.  The picture frame in the left hand image is approximately 30 centimetres. 

CED_Vaucheria_May19

Cell walls of Vaucheria, with a few chloroplasts still present, from Castle Eden Burn, May 2019.  Scale bar: 20 micrometres (= 1/50thof a millimetre). 

However, the structures did not really match any pictures that I could find of oogonia or antheridia in Vaucheria.  I passed my images around some friends, and Gordon Beakes suggested that we might be looking at sporangia of chytrids, a group of fungi that have a string of previous convictions for infecting algae (see “Little bugs have littler bugs upon their backs to bite ‘em ….”).  As I was taking the photographs below, a cloud of tiny spores was released, prompting me to call out “come quickly if you want to see an alga ejaculating” before remembering that we had visitors in the house who might think this a little weird (and not just because I had not yet realised that they were, in fact, fungi).   I even took a video.  I’ll upload it to the Dark Web at some point.  There must be a site for fungal-themed pornography out there, if only I took the time to look…

CED_Vaucheria_oospores

Sporangia of chytrids on Vaucheria filaments from Castle Eden Burn, May 2019.  The one on the right was releasing spores (arrowed) at the time the photograph was taken.   Scale bar: 20 micrometres (= 1/50thof a millimetre).  

Who do you think you are?

As well as the diatom growths, the bed of the River Browney was also covered with skeins of a green-coloured alga which, when I removed it, had a soft, felt-like texture.   This is Vaucheria, a very common constituent of enriched rivers in Britain.   Under the microscope, the filaments can be seen to be long tubes (think of sausage skins) within which there are numerous tiny green chloroplasts.   This is not the first bright green alga that I have written about in this blog but appearances, in the world of algae, can often be deceptive.

Browney_Vaucheria

We often see the evolutionary history of life on earth portrayed as a tree whose branches, representing each of the main groups of organisms, diverge again and again, culminating in “twigs” representing each species.   Following any “twig” back towards the “trunk” links to successively larger groupings of organisms.   So, for example, the species to which we belong, Homo sapiens, has no very close relatives, but is linked at the next level (family) to apes such as the chimpanzee.  Humans and chimps are, in turn, linked to the primates (order) such as gibbons and lemurs, which are part the mammals (class), including elephants and lions, which is part of the chordata (phylum) which links us to fish and reptiles.   Finally, the chordate belong to the Animalia (Kingdom) which links us to flies and slugs, and Animalia is part of the Domain Eukaryophyta, which links us to the rest of life except for bacteria.

We can use this analogy to express the relationship between any two organisms in terms of the number of steps along the tree before we find a common relative.  If we compared Vaucheria to Bulbochaete, which we met on 16 August, another bright green growth from the bed of a river, surprisingly we have to take eight steps (equivalent to comparing humans with plants!).   By contrast, the distance between Bulbochaete and Spirogyra is six steps (humans v fish) and between Vaucheria and Melosira (4 September) is a mere four steps (humans v gibbons).

The message is that the affinities amongst the algae are often not best discerned through seemingly obvious characteristics such as colour and shape but through biochemical composition, similarities in reproduction and the life cycle and in the structure of the DNA.  The other message is that the umbrella term “algae”, usually bit-players in any consideration of life on earth, embraces as much diversity as a typical zoo.   This is too easily forgotten, at least in part because they lack the televisual qualities that lend themselves to wildlife documentaries.   Unfortunately, in the process, we also often lose sight of the importance of algae in ecosystems.

Note

There is no universally agreed system of higher classification (see post of 11 August).  For this exercise I used the tree of life project (www.tolweb.org) as the basis for the classification of animals and Algaebase (www.algaebase.org) for the algae.