Stealing the Ability to Photosynthesize and Endosymbiotic Theory

by AS

Have you ever wondered whether we could use genetic engineering to make an organism capable of photosynthesis, or maybe just how plants gained the ability in the first place? Well, studying the unique food chain of Dinophysis acuminata is helping to provide answers for questions like these. Dinophysis acuminata is a unicellular marine plankton that feeds on a ciliate plankton called Myrionecta rubra, which in turn feeds on photosynthetic algae like Geminigera cryophila. What makes this food chain interesting is all three of these species perform photosynthesis, but the two predators do it by using the cellular machinery of their prey. That is to say, rather than consuming the whole of their prey, they conserve the chloroplasts and even the genetic information necessary for chloroplast maintenance so they can perform photosynthesis. However, before we dive into the deep end of life as a plankton in the ocean, we need to discuss endosymbiotic theory. Endosymbiotic theory will reveal why this food chain adds to our understanding of evolution and what genes are necessary for photosynthesis.

To begin, cells are divided into two groups, prokaryotes and eukaryotes. All cells possess a plasma membrane dividing them from the environment, but eukaryotes are known for having internal membranes as well. These internal membranes segregate portions of the cell into compartments, called organelles, where specialized cellular functions occur. One of these organelles, the chloroplast, is what allows photosynthetic organisms to capture energy from light and store it in the form of carbohydrates, like glucose.

It’s thought chloroplasts evolved through endosymbiosis, whereby one cell, known as an endosymbiont, lives within another (Chan & Bhattacharya, 2010). The idea is a unicellular predator engulfs a cell that can photosynthesize and, instead of digesting its prey, the predator keeps the prey within it. This allows the predator, which is now the host, to feed off sugars generated by the engulfed photosynthetic cell for an extended period of time. This arrangement can also benefit the endosymbiont in numerous ways. The most obvious advantage being it is now protected from other less accommodating predators. In addition, the endosymbiont is now shielded from some environmental stresses by the host’s plasma membrane, such as harsh chemicals.

Over time, and many generations, the endosymbiont’s genome shrinks and populations of them start getting passed from parent host cells directly to the host cell’s progeny. This is opposed to progeny needing to find and engulf their own endosymbionts. Genes are transferred from the endosymbiont’s genome to the host’s with astounding frequency while other, no longer essential, genes are simply lost (Timmis et al., 2004). At a certain point, the once free-living endosymbiont no longer contains within its genome the genes necessary to survive on its own, because these genes have been transferred to the host nucleus. At this point the endosymbiont has been reduced to an organelle and has become a part of the host, rather than a partner.

Most of the endosymbiont’s genome shrinkage is believed to occur soon after the endosymbiont begins living within its host. However, keep in mind that is ‘soon’ on an evolutionary timescale, which implies millions of years. It’s been found gene transfer from organelle to host nucleus is an ongoing process and, surprisingly, many of the protein products encoded by the transferred genes are not targeted back to the organelle those genes originated from (Archibald, 2005). For instance, one study concluded about 18% of genes within the genome of the plant Arabidopsis thaliana originated from cyanobacterial endosymbionts, and less than half of the protein products of those genes were targeted to chloroplasts (Archibald, 2005). This implies gene transfer from endosymbionts has played a large role in shaping the evolution of higher eukaryotes. Since many of these transferred genes don’t associate directly with the chloroplasts they originated from anymore, this influence likely goes beyond just contributing genes involved with maintaining organelles and their cellular processes. That’s fascinating, and implies the acquisition of permanent chloroplasts was a monumental step in the evolution of eukaryotes for reasons beyond the obvious; they provided the basis for multicellular photosynthetic organisms.

Generally, it’s agreed this critical step in the evolution of eukaryotes only occurred once and all chloroplasts evolved from a single photosynthetic cyanobacterium that formed an endosymbiotic relationship with a common ancestor of all photosynthetic eukaryotes (Archibald, 2005). This is called the primary endosymbiotic origin of chloroplasts. The problem with studying this process, and the effects it’s had on eukaryotic evolution, is these events happened billions of years ago (Archibald, 2005). However, there is another level of this process we can study because it’s still ongoing today.

Secondary endosymbiosis begins with a non-photosynthetic eukaryote engulfing a eukaryote that contains some method of photosynthesizing; whether it be endosymbiotic bacteria, chloroplasts, or something in between. The predator then digests the engulfed eukaryote but keeps the photosynthesizing apparatus for itself. The number of times secondary endosymbiosis has resulted in new species with permanent chloroplasts is still debated, but there is strong evidence that it has occurred at least three times (Archibald, 2005).

Now the process of permanently acquiring chloroplasts via secondary endosymbiosis is slightly different from that undergone during the primary endosymbiotic origin. Chloroplasts no longer contain all of the genes necessary for photosynthesis or self-maintenance (Archibald, 2005, Johnson et al., 2007). Remember, large portions of the organelle’s genome were transferred to the host nucleus, and the host was just digested. This means stolen chloroplasts eventually break down and stop producing energy for their new host. In order to extend the lifetime of their stolen goods, the new host must acquire the missing genes from other eukaryotes that already keep a stable population of chloroplasts.

An excellent example of secondary endosymbiosis is the food chain of D. acuminata discussed earlier. Starting at the bottom, M. rubra engulfs algae and digests them, but keeps their chloroplasts and nuclei. Now the cool thing is the nuclei of the digested algae accumulate within M. rubra and remain transcriptionally active. Transcription is the process of turning genes into mRNA, which is translated into the proteins that mediate cellular processes, like photosynthesis. So the stolen algal nuclei continue to produce the mRNA that encode the proteins needed for maintaining chloroplasts and driving photosynthesis. However, the nuclei do have a 10-day half-life within M. rubra so it needs to feed continuously to maintain its stolen chloroplasts. (Johnson et al., 2007)

The journey of our pilfered chloroplasts doesn’t stop there however. D. acuminata feeds off M. rubra and keeps the now twice appropriated chloroplasts for itself. Unlike M. rubra, D. acuminata does not keep the original host nuclei. Yet, D. acuminata can keep their chloroplasts for months without feeding. This is possible because D. acuminata has somehow acquired several genes from algae that regulate and maintain chloroplasts. Five such genes have been identified. What makes this even more interesting is only one of them originates from a cryophyte, which are photosynthetic organisms that can live on snow or ice, such as the original owner of the chloroplasts G. cryophila (Wisecaver & Hackett, 2011). You would expect the new host to acquire the necessary genes from the original host, its prey, and this has been found to be the case with other dinoflagellates that steal their chloroplasts like D. acuminata. However, the other 4 identified genes came from algal lineages different from G. cryophila. D. acuminata obtained these algal genes through some form of horizontal gene transfer (HGT). HGT is simply defined as the transfer of genetic material between organisms that occurs through routes other than parent to offspring, which is vertical gene transfer. For example, the transfer of genes from endosymbiont to host we’ve been discussing is a form of HGT.

Thus, this food chain offers two very different approaches to maintaining chloroplasts acquired from prey. M. rubra’s method of stealing whole nuclei has never been observed before, and therefore represents a unique research opportunity. Also, since M. rubra collects the nuclei of its prey, they are frequently exposed to the genes necessary for maintaining chloroplasts permanently. Many researchers have suggested M. rubra is in the process of taking these genes into its genome and permanently acquiring chloroplasts (Johnson et al., 2006).

Meanwhile, D. acuminata employs a more haphazard approach to endosymbiosis. Since it goes through M. rubra as an intermediary for its chloroplasts, D. acuminata is exposed to the genome of the original host less frequently. Some have postulated this is why most of D. acuminata’s genes involved with chloroplast maintenance originate from sources other than the original host. It simply doesn’t have access to the original host’s genome very often so the opportunity for HGT doesn’t arise. The actual mechanisms of HGT aren’t well understood in eukaryotes though, and D. acuminata could serve as a model for further investigation concerning eukaryotic HGT as well as secondary endosymbiosis (Zhaxybayeva & Doolittle, 2011).

For these reasons both M. rubra and D. acuminata are amazing organisms that may very well provide insights into how the process of endosymbiosis produced modern eukaryotes and continues to influence their evolution today. In addition, by observing the process of HGT in these organisms and the impact of specific genes, we could determine the specific gene set necessary to permanently sustain chloroplasts. Genetically engineering photosynthetic organisms may seem straight out of sci-fi, but with a list of necessary genes and modern genome editing tools it may not be too far away. However, don’t hold your breath. You can’t generate your own oxygen just yet.

References:

-       Archibald, J. M. (2005). Jumping Genes and Shrinking Genomes - Probing the Evolution of Eukaryotic Photosynthesis with Genomics. IUBMB Life, 57(8), 539–547. https://doi.org/10.1080/15216540500167732.

-       Chan, C. X. & Bhattacharya, D. (2010) The Origin of Plastids. Nature Education 3(9):84.

-       Johnson, M. D., Tengs, T., Oldach, D. and Stoecker, D. K. (2006), SEQUESTRATION, PERFORMANCE, AND FUNCTIONAL CONTROL OF CRYPTOPHYTE PLASTIDS IN THE CILIATE MYRIONECTA RUBRA (CILIOPHORA)¹. Journal of Phycology, 42: 1235–1246. doi:10.1111/j.1529-8817.2006.00275.x

-       Johnson, M. D., Oldach, D., Delwiche, C. F., & Stoecker, D. K. (2007). Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature, 445(7126), 426–428. https://doi.org/10.1038/nature05496.

-       Timmis, J. N., Ayliffe, M. A., Huang, C. Y., & Martin, W. (2004). Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet, 5(2), 123–135. https://doi.org/10.1038/nrg1271.

-       Wisecaver, J. H., & Hackett, J. D. (2010). Transcriptome analysis reveals nuclear-encoded proteins for the maintenance of temporary plastids in the dinoflagellate Dinophysis acuminata. BMC Genomics, 11, 366. http://doi.org/10.1186/1471-2164-11-366.

-       Zhaxybayeva, O., & Doolittle, W. F. (2011). Lateral gene transfer. Current Biology, 21(7), R242–R246. https://doi.org/10.1016/j.cub.2011.01.045.