Tuesday, February 7, 2012

Into the Ocean Without a Paddle - the Mystery of the Red Algae

Most red algae, like this
Batrachospermum, are complex,
multicellular seaweeds (though
this is a freshwater genus).  From
Oltmanns, Morphologie und Biology
der Algen. 1922, Fig.469. 
The term "algae" refers to a wide range of simple aquatic organisms that have chloroplasts.  The red algae are a distinct and natural ("monophyletic") group of algae with reddish pigments in their chloroplasts similar to those of the cyanobacteria.  They are believed to be directly descended from the first eukaryotes to incorporate cyanobacteria as proto-chloroplasts (see my posting "Plants, animals and kleptoplasts, oh my").  The green algae (which later would give rise to the land plants)  have different chloroplast pigments that are an adaptation for life in shallow water.  Though it is not totally settled, DNA evidence suggests that red and green algae are closely related and that the green algae are also directly descended from the first organisms with chloroplasts.  The two groups are believed to have split apart very early on.  The rest of this article assumes that this relationship is true, and explores the mysteries that result from it.

While green algae have varied growth forms, the red algae are mostly complex, multicellular seaweeds.  Seaweeds, like their photosynthetic cousins on land, are organisms that set down "roots" in a suitable location, and stay put for the rest of their life.  But being glued to one spot makes it even more important that they have a means to disperse their genetic information during their reproductive cycles.  In algae, that's typically a 2-step process: spores that travel long distances to mingle with other populations, and sperm cells to travel relatively shorter distances to seek out a suitable egg (see "The truth about sex in plants").  For that they need some means of locomotion, and for single-celled organisms that usually means slender whip-like organelles called flagella (or cilia, which are smaller, but of the same structure). 

They mystery of the red algae arises from the fact that neither their sperm cells nor their dispersal spores have flagella.   Such cells are literally adrift in the ocean "without a paddle."  Throughout this entire group there is no sign of flagella in any species or in any part of the life cycle.  There is no sign even of the flagella-supporting structures (centrioles), usually found in all cells (not just cells with flagella) in other algae and land plants.  It is as if the ancestors of red algae never had flagella at all.  That hypothesis is however complicated by the apparent relationship of red and green algae and their common descent from the first photosynthtic eukaryotes. 

In the unicellular Chlamydomonas, all cells (except for the
dormant zygote) have two flagella.  In multicellular green algae,
only the gametes and zoospores are so equipped. 
From Haupt, Plant Morphology, 1953, Fig. 16.
Flagella are found throughout the eukaryotic domain: in animal and plant sperm cells, in single-celled protists like paramecia and trypanosomes (vectors of sleeping sickness and other diseases), and in the zoospores and sperm cells of most (non-red) algae.  Flagella apparently evolved among the earliest eukaryotes, for their structure is fundamentally the same wherever we find them.  Most green algae produce sperm cells and zoospores with flagella exhibiting that ancient and universal structure.  So the common ancestor of red and green algae must have had flagella.

So the mystery has several layers, including a dilemma: red algae have the older form of chloroplast, and presumably came first, with the green algae evolving from them.  But green algae have the original mode of locomotion provided by flagella, and the flagella-less red algae must have evolved from them!  The simple solution to this is that the first algae had red chloroplasts and flagella, and subsequently split into two groups.  Red algae as we know them today have the original chloroplast but have lost their flagella.  The green algae evolved a new type of chloroplast but retained flagella.

But now we have to ask "why did red algae lose their flagella?"  How do their sperm cells find eggs without any means of self-directed movement?  Textbooks are vague on this issue, generally implying that the loss of flagella must have been accidental.  But it seems that the elimination of flagella and associated support structures, indeed all the genes involvd in producing flagella, was ruthlessly thorough and therefore must have happened for some adaptive "reason."

In red algae such as this Polysiphonia, tiny dust-like sperm cells, called spermatia, are released in great numbers from male plants. As the spermatia swirl around in the water, they are caught by the egg-producing structure on a female plant by long projections called trichogynes. Modified from Raven et. al, Biology of Plants, ed. 7, 2005.
I believe the reason was a change of strategy similar to the shift to wind-pollination in grasses or oaks.  Red algae sperm cells are tiny, barely more than a nucleus.  They are stripped down like this because they don't require the apparatus or energy reserves for locomotion.  They can be produced more cheaply and in much greater numbers.  By releasing huge quantities of tiny sperm cells, red algae are banking on the chance that some of them will randomly drift to the vicinity of egg-producing structures and get caught on them.  This is similar to the grass strategy of producing vast quantities of tiny pollen grains, a few of which get caught in the feathery stigmas of the female pistils.  Grasses exist in large populations in open, windy habitats where this strategy works well.  Presumably, red algae live where similar underwater currents produce the same results.  Green algae, on the other hand, may have evolved in quieter waters, where flagella were still necessary for successful dispersal.