By Vidya Rajan, Columnist, The Times
In an earlier article[1] I wrote about tardigrades, a ubiquitous and indestructible animal with an extraordinary ability to endure adverse environmental conditions. This superpower is assisted by their entry into a dormant state called “tun”, in which they lose all their water and curl up into a husk. Tardigrades in the tun state can be subjected to boiling, freezing, radiation, high pressures, immersion in toxins, and even endure short periods in outer space without apparent problems. When rehydrated, they resume their activities as normal. Their DNA is as odd as they are: one-sixth is scavenged from other organisms: archaea, bacteria, fungi, and plants.[2] Tardigrades are not alone in purloining genes from other organisms. In this article, I will examine life forms which have gathered unto themselves genes which presumably give them an advantage in the competition for survival. Then I will briefly glance at humans, since our DNA also contains genes of foreign origin.
A short introduction: The DNA of a cell represents the “genotype” which is the blueprint for the characteristics of the tangible body, whereas the term “phenotype” describes the physical form that interacts with the environment. It is the phenotype which either survives and reproduces successfully (thereby passing on the genotype that encodes the physical and mental aspects determinative of success), or it is outcompeted and dies without producing offspring. The ecosystem includes the environment and other organisms as collaborators, predators or prey. Bacteria can release DNA actively by “blebbing”[3] from living and DNA from broken cells of any origin can escape into the environment. Living cells can occasionally pick up and incorporate this naked DNA from the environment into their own chromosomes; the process is known as “horizontal gene transfer”. The spread of antibiotic-resistance genes is only the tip of the iceberg. Horizontal gene transfer allows host cells in the digestive lining, or symbionts within the digestive tract, to also pick up foreign DNA. Not all of the DNA taken up makes it into another organism’s cell, and not all of the entering DNA is incorporated into the genome. It is assumed that there is a survival advantage (even if all of the mechanisms have not been teased out) to retain sequences obtained this way; if there were no benefit, the costs of their maintenance would exert pressure to jettison freeloaders. Even rare uptake can have a profound effect on an organism if it contains a gene that has survival value.
Examining genomes shows that gene snatching is pretty common between prokaryotes such as bacteria, but it has also been found in eukaryotes, including invertebrate and vertebrate animals, fungi and plants.[4] For example:
Cellulases from bacteria to nematodes: [5] Plant-munching roundworms called nematodes have incorporated functional cellulases into their genome on several distinct occasions. Not only that, the cellulase genes have then been modified by duplication and the incorporation of typically eukaryotic motifs such as introns. This domestication points to the value that cellulases provide to nematodes in their parasitism of plants.
Antibiotic genes from bacteria into a variety of eukaryotes: [6],[7] Across the eukaryotic domain: protozoa, arthropods, mollusks, and even a primitive vertebrate, have incorporated antibiotic genes of bacterial origin called “dae” – the “d” stands for domesticated. These genes are functional in their new hosts, helping them to overcome bacterial infections. One specific, fascinating, example is the mite (Ixodes scapularis) that transmits Lyme disease caused by the bacterium Borrelia burgdorferi. When a mites sucks in Lyme-bacteria tainted blood, dae proteins in its system keep the bacteria in check and prevent it from infecting the mite itself. The mite then merrily passes on the bacteria with its next blood meal.
Color genes from fungi by aphids: [8] Aphids are a bunch of sap-sucking insects which gardeners typically wage war upon. They come in many colors with their pigmentation typically coming from the food they consume; but the green and red colors of pea aphids and potato-peach aphids has an unusual origin story: their common ancestor stole their carotenoid genes from a fungus. Subsequently, green aphids began expressing the yellow carotene variant of the genes, and the red aphid expresses two red carotenoid genes that the green variant lacks. It seems that, after incorporating two fungal carotenoid genes, the green aphid and the red aphid tinkered with them independently. The green aphid jettisoned a gene that converts yellow carotene to red carotene, whereas the red aphid retained them, with differential survival outcomes: green aphids are typically attacked by parasitic wasps, whereas red aphids are targeted by ladybugs. In other words, green aphids are spared by ladybugs, and red aphids avoid parasitic wasps.
Viruses by parasitic wasps: [9] Parasitic wasps themselves have a secret: their predatory ability comes from hijacking a virus whose genes they incorporated into their own genome. Parasitic wasps lay their eggs in the bodies of living insect hosts. The egg develops into a grub and eats the host’s tissues, hollowing it out but sparing vital organs until the very end. But insects have immune systems to repel invaders, so the wasp produces these virus particles (themselves an amalgamation of assembled from shells of nudiviruses and DNA from polydnaviruses) which suppress the host insect’s immune system, allowing the egg to hatch and the grub to develop. The wasp allows the polydnavirus to replicate in order to infect the host and suppress its immune system, and this suppressed host allows the wasp to produce offspring. They are thus locked into a mutually dependent relationship for survival.
Russian doll mealybugs: [10] Ensconced inside a citrus mealybug is a bacterium called Tremblaya princeps, and sheltering within the cells of T.princeps is another bacterium called Moranella endobia. M.endobia makes amino acids from precursors, supporting both T.princeps and the mealybug. This simple bug-inside-bug-inside-bug masks more complexity: T.princeps appears to have ceded many of its genes to the mealybug, becoming a middleman, supported by its investments rather than by any effort it exerts. Meanwhile the mealybug has industriously collected a bunch of other bacterial genes presumably from other bacterial symbionts and steams on.
Bacterium-gene wielding, coffee-munching beetle: [11] The coffeeberry-borer larvae uses digestive genes that it usurped from bacteria that make enzymes called mannanase to metabolize an unusual carbohydrate called galactomannan found in coffee. This success has spread the coffee borer around the world to consume the beans that are grown commercially, to the detriment of coffee growers.
SPIN genes in vertebrates: [12] SPIN stands for Space Invaders, a whimsical name for a gene that has jumped from bacteria to an unrelated collection of vertebrates: green anoles, African clawed frogs, little brown bats, mouse, rat, opossum and tenrecs. Thus this gene did not jump to an ancestor of all these animals but appears to have been acquired many times, independently. SPIN is a jumping gene, or transposon. But this is a transposon that recruits viruses to go from one species to another, and the specific virus is a poxvirus with a broad infection spectrum that includes all the animals playing host to SPIN. Within each host, SPIN has copied itself into the genome multiple times (4,000 copies in the African clawed frog to 99,000 times in the tenrec). But what SPIN does is a mystery.
Wolbachia in insects: [13] A parasitic bacterium called Wolbachia infects all sorts of insects from fruit flies to dragonflies. Its ubiquity is remarkable – it is reportedly found in about 50% of all insects conferring a slew of reproductive phenotypes such as the ability to reproduce without sex (parthenogenesis), feminization, asexuality and reduced embryo viability, all the way to pathogen blocking. In fruit flies, the Wolbachia bacterium has sidestepped the problem of infecting successive generations from scratch – it has transferred its entire genome into the fruit fly, such that every cell contains it. It’s a remarkable strategy, because it is energy-intensive for hosts to support parasites. In another twist, mosquitoes that contain Wolbachia transmit viruses that cause dengue and zika much less effectively than Wolbachia-free mosquitoes. Therefore, increasing Wolbachia prevalence in mosquitoes reduces viral transmission, and is making an effective strategy in dengue- and zika-endemic areas. This approach could be expanded to other viruses (chikungunya, yellow fever, West Nile virus) and to protozoa (malaria-causing Plasmodium and sleeping sickness-causing Trypanosoma) by inserting mosquito-sterility genes into Wolbachia that it will dutifully transfer to its host. Ideas of expanding from mosquitoes to agricultural pests are also in the pipeline. [14]
In the solitary Hymeoptera (which includes bees, wasps and ants) Wolbachia has been associated with the ability of unmated females to lay diploid eggs which develop into females (an unusual parthenogenetic ability called thelytoky) or haploid eggs which develop into males (arrhenotoky, a typically present ability in haplo-diploidy). It is thought that arrhenotoky developed from thelytoky, driven by the presence of Wolbachia and similar endobacterial symbionts (although it is occasionally genetically driven [15]). Wolbachia has been found in Apis (honeybee), and Bombus (bumblebee) as well as in the ectoparasite, Varroa destructor. Preliminary work shows that Wolbachia increases transmission of deformed wing virus (DWV) by Varroa mites.[16]
This evolutionary openness to incorporate others’ genes is similar to tool use or cultural learning; the item or information can be modified and used for both beneficial and detrimental outcomes. At this time, the answer to whether Wolbachia is beneficial or detrimental to social bees is not clear. [17]
Bibliography:
[1]. Rajan, V. (2022) Inner Nature: The incredibly resilient tardigrade. The Unionville Times. [online] Available at: https://www.unionvilletimes.com/?p=49770
[2]. Yong, E. (2015) Inside the Fascinating Genome of the World’s Toughest Animal, in The Atlantic. https://www.theatlantic.com/science/archive/2015/11/tardigrades-worlds-toughest-animals-borrowed-a-sixth-of-their-dna-from-microbes/417243/
[3]. Velimirov, B. and Ranftler, C., 2018. Unexpected aspects in the dynamics of horizontal gene transfer of prokaryotes: the impact of outer membrane vesicles. Wiener Medizinische Wochenschrift (1946), 168(11), p.307.
[4]. Ed Yong, the Pulitzer-prize winning science writer has written several articles about horizontal gene transfer with his characteristically engaging and accessible writing. Check out https://www.nationalgeographic.com/science/article/a-flood-of-borrowed-genes-at-the-origins-of-tiny-extremists
[5]. Mayer, W.E., Schuster, L.N., Bartelmes, G., Dieterich, C. and Sommer, R.J., 2011. Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover. BMC evolutionary biology, 11, pp.1-10.
[6]. Husnik, F. and McCutcheon, J.P., 2018. Functional horizontal gene transfer from bacteria to eukaryotes. Nature Reviews Microbiology, 16(2), pp.67-79. DOI: https://doi.org/10.1038/nrmicro.2017.137
[7]. Yong, E. (2014). Raiding the Oldest Arsenal. [online] Science. Available at: https://www.nationalgeographic.com/science/article/raiding-the-oldest-arsenal [Accessed 4 Aug. 2024].
[8]. Yong, E. (2010). Aphids got their colours by stealing genes from fungi. [online] Available at: https://www.nationalgeographic.com/science/article/aphids-got-their-colours-by-stealing-genes-from-fungi. [Accessed 4 Aug. 2024]
[9]. Yong, E. (2009). Wasps use genes stolen from ancient viruses to make biological weapons. [online] Science. Available at: https://www.nationalgeographic.com/science/article/wasps-use-genes-stolen-from-ancient-viruses-to-make-biological-weapons [Accessed 4 Aug. 2024].
[10]. Yong, E. (2013). Snug as a Bug in a Bug in a Bug. [online] Science. Available at: https://www.nationalgeographic.com/science/article/snug-as-a-bug-in-a-bug-in-a-bug [Accessed 4 Aug. 2024].
[11]. Yong, E. (2012). Beetle pest destroys coffee plants with a gene stolen from bacteria. [online] Science. Available at: https://www.nationalgeographic.com/science/article/beetle-pest-destroys-coffee-plants-with-a-gene-stolen-from-bacteria [Accessed 4 Aug. 2024].
[12]. Yong, E. (2008). Space Invader DNA jumped across mammalian genomes. [online] Science. Available at: https://www.nationalgeographic.com/science/article/space-invader-dna-jumped-across-mammalian-genomes [Accessed 4 Aug. 2024].
[13]. Yong, E. (2009). An entire bacterial genome discovered inside that of a fruit fly. [online] Science. Available at: https://www.nationalgeographic.com/science/article/an-entire-bacterial-genome-discovered-inside-that-of-a-fruit-fly [Accessed 4 Aug. 2024].
[14]. Caragata, E.P., Dutra, H.L., Sucupira, P.H., Ferreira, A.G. and Moreira, L.A., 2021. Wolbachia as translational science: controlling mosquito-borne pathogens. Trends in parasitology, 37(12), pp.1050-1067. PDF available at: https://www.sciencedirect.com/science/article/am/pii/S1471492221001641
[15]. Mumoki FN, Yusuf AA, Pirk CWW, Crewe RM (2021) The Biology of the Cape Honey Bee, Apis mellifera capensis (Hymenoptera: Apidae): A Review of Thelytoky and Its Influence on Social Parasitism and Worker Reproduction. Annals of the Entomological Society of America, Volume 114, Issue 2, Pages 219–228, https://doi.org/10.1093/aesa/saaa056
[16]. Grau, T., Brandt, A., DeLeon, S., Meixner, M.D., Strauß, J.F., Joop, G. and Telschow, A., 2017. A comparison of Wolbachia infection frequencies in Varroa with prevalence of deformed wing virus. Journal of Insect Science, 17(3), p.72. DOI: https://doi.org/10.1093/jisesa/iex039
[17]. Ramalho MdeO, Kim Z, Wang S, Moreau CS (2021) Wolbachia Across Social Insects: Patterns and Implications, Annals of the Entomological Society of America, Volume 114, Issue 2, March 2021, Pages 206–218, https://doi.org/10.1093/aesa/saaa053
