Walking Cells and Other Surprises Among Protists — An Evolutionary Challenge
The world of protists is expanding at a fast clip. New eukaryotic microbes are being discovered, some with little or no known connection to identified species. Taxonomists are not sure how to classify them. Some are even willing to create new phyla, supergroups, or kingdoms to house them. Three commentators in Current Biology expressed the surprise:
Probably more scientists study sparrows than all the free-living microbial eukaryotes (protists) combined. This is quite unfortunate, not because the former are unworthy, but because the latter not only contribute substantially to planetary health, but they also represent the majority of functional and evolutionary eukaryotic diversity on Earth. This fact usually comes as a surprise to people studying macroscopic eukaryotes, yet the diversity of protists is bound to grow even further, as implied by the fact that 50% of eukaryotic genes expressed in the ocean do not have any match in public databases and/or lack any reliable phylogenetic affiliation.
Let’s examine two new species identified recently. Imagine protists that walk on legs like bugs, or paddle with arms. How do they do it? Where did they come from? And must the commentators beg the question of evolution in the phrase “evolutionary eukaryotic diversity” instead of just describing “eukaryotic diversity”? These two protists possess only distant morphological similarities to other members of their taxa, so imagining a phylogeny between them seems strained. For now, behold and wonder!
Meteora sporadica: The Paddling Hunter
This creature is so weird, you have to watch it in motion to believe it. The cell body is slightly elongated, and from the major axis two long filaments extend twice its body length forward and backward. This is the axis along which it glides with cilia. But now, picture “arms” extending out to the sides that paddle back and forth, one sweeping forward while the opposite arm sweeps backward.
It’s rare to find the word “incredible” in a formal scientific paper’s title, but Eglit et al., writing in the same issue of Current Biology, must have been astonished when they announced this creature as “a protist with incredible cell architecture.”
“Kingdom-level” branches are being added to the tree of eukaryotes at a rate approaching one per year, with no signs of slowing down. Some are completely new discoveries, whereas others are morphologically unusual protists that were previously described but lacked molecular data. For example, Hemimastigophora are predatory protists with two rows of flagella that were known since the 19th century but proved to represent a new deep-branching eukaryote lineage when phylogenomic analyses were conducted. Meteora sporadica is a protist with a unique morphology; cells glide over substrates along a long axis of anterior and posterior projections while a pair of lateral “arms” swing back and forth, a motility system without any obvious parallels.
For those without access to the paper with its videos of this protist, the only YouTube video I could find is a short one with very loud music, so you might want to quiet your device before viewing this otherwise good look at M. sporadica in action.
This creature’s motility suggests more complexity under the hood. The authors say it has the most gene-rich mitochondrial genome among protists. The “arms” that swing back and forth are made of bundles of microtubules, which grow from unique subnuclear microtubule organizing centers (MTOCs) that are unlike the more familiar axonemes of cilia. Surprisingly, this protist can move without the “arms” but gets along faster with them.
Bumps are visible along the lateral arms; what are those? They are called extrusomes. These granules can move up and down along the arms and can be “fired” at bacterial prey. Once it surrounds the target, the extrusome delivers the bacterial burrito to a food vacuole where it is phagocytosed (digested).
Like all other eukaryotes, M. sporadica is equipped with organelles: a nucleus, mitochondria, longitudinal bundles of microtubules, and molecular motors like dyneins to animate the microtubules. Of course, it also contains all the machinery for metabolism, mitosis, DNA storage, transcription, and translation, in addition to motility. This is no simple animal.
Euplotes, a Microbial Cockroach
Seen from the side, this protist looks like a cockroach or pill bug scooting along the floor, but it is much tinier. Insects have legs made of cells. This protist is a single cell. How can it sprout legs and walk? Take a look at it under the microscope on this YouTube video (again, the music contributes little). The side view at 1:08 shows its resemblance to a walking bug. Investigators Laeverenz-Schlogelhofer and Wan, writing in the same issue of Current Biology, are amazed at the uncanny similarity to animal behavior on a vastly different scale.
Diverse animal species exhibit highly stereotyped behavioral actions and locomotor sequences as they explore their natural environments. In many such cases, the neural basis of behavior is well established, where dedicated neural circuitry contributes to the initiation and regulation of certain response sequences. At the microscopic scale, single-celled eukaryotes (protists) also exhibit remarkably complex behaviors and yet are completely devoid of nervous systems. Here, to address the question of how single cells control behavior, we study locomotor patterning in the exemplary hypotrich ciliate Euplotes, a highly polarized cell, which actuates a large number of leg-like appendages called cirri (each a bundle of ∼25–50 cilia) to swim in fluids or walk on surfaces.
The paper describes the coordination between the cirri (sing. cirrus) when the protist moves. There are 10 frontoventral cirri and 5 transverse cirri arranged in an asymmetrical pattern, plus 4 caudal cirri at the tail end. “Distinct cirri are involved in generating distinct gaits,” the authors observe. Each cirrus moves with a power stroke and recovery stroke, like a swimmer. The cilia that line our airways move in a similar fashion, but in Euplotes they stroke in large bundles. Like other ciliates, these protists are well equipped with numerous other individual cilia that control the movement of food to their vacuoles. “These organisms are among the most morphologically complex and differentiated groups of ciliates,” remark Laeverenz-Schlogelhofer and Wan.
The authors identified three stereotypical movements performed by Euplotes with their cirri: the swim, the forward walk, and the sidestep reaction (SSR). The first two strategies allow the protist to move forward. The SSR allows it to quickly back up and turn. While swimming, the asymmetrical pattern of cirri makes it rotate in a helical fashion. But while walking on a surface (like the cover slip of a microscope slide), it scoots along like a cockroach. The authors notice the functional purpose of cirri when they describe them as “compound leg-like structures comprising many cilia.”
In higher animals, movement is powered by muscles in response to neural signals. The “legs” of these microbes are electrically powered. Specifically, calcium ions flowing through channels in the membrane create cycles of polarization and depolarization about every half second. A slight delayed response shows the cirri decelerating during depolarization and speeding up during polarization. Overall, though, the motion is fairly uniform and rapid. High speed videography allowed the researchers to monitor the actions in slow motion; otherwise the pauses would hardly be noticeable.
Implications
It’s exciting to ponder that the world is filled with examples of cellular motility beyond the iconic bacterial flagellum — and we probably don’t know even half of what exists. While ciliates such as Vorticella, Stentor, and Paramecium have been well known since Van Leeuwenhoek wrote about the “wee beasties” that he saw “very prettily a-moving” under his crude microscopes, many more remain to be identified. These two examples were found in shallow marine sediments. Some of the newly discovered microbes are common in our own backyards, in soil or puddles. The fact that many of them show no clear phylogenetic connection with other microbes, and may contain unique morphological structures, poses a severe challenge to Darwinism. The more isolated diversity, the weaker the argument for common ancestry.
We intuitively appreciate the form and function of legs in Euplotes and arms in Meteora even though they are profoundly smaller than ours. A “leg” on Euplotes differs in size by six orders of magnitude from the leg of Brachiosaurus, yet both perform the function of motility. Each limb’s design, further, is suited for its habitat and for the physical forces required. The more unique purposeful motion is discovered, the more the evidence that the biosphere has been engineered for action.
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