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Interdomain Interactions: Dissecting Animal–Bacterial Symbioses

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Interdomain Interactions: Dissecting Animal–Bacterial Symbioses Feature Interdomain Interactions: Dissecting Animal–Bacterial Symbioses Downloaded from https://academic.oup.com/bioscience/article/56/5/376/234704 by guest on 01 October 2021 MELISSA LEE PHILLIPS or the first billion years of life on FEarth, prokaryotes had the place to themselves. By the time the first eukary- otes and then, finally, multicellular or- ganisms arose and diversified, prokaryotic bacteria and archaebacteria had invaded almost every nook of the planet and in- vented nearly every known metabolic pathway. “All the animal body plans evolved in a microbe-rich marine environment,” Immature individual of the spittlebug Clastoptera arizonana, showing says developmental biologist Margaret the brightly colored bacteriomes on each side of the abdomen. Two McFall-Ngai of the University of different symbionts live in this insect: Candidatus Sulcia muelleri and an Wisconsin–Madison.“It’s very likely that unnamed species of ß-proteobacteria. Photograph: Phat Tran. it was a very common thing to associate with microorganisms.” toxin that wards off wolf spiders, and to offspring through the egg cell, while Selective pressure from other organ- several insects have symbionts that con- bacteria that live outside host cells are isms has come not only from creatures fer resistance to extreme heat. usually picked up from the environment evolving alongside them but, in many Some symbiotic bacteria colonize host by each new generation of animals. In cases, from inside of them. Virtually all epithelial tissue, such as the mammalian some animal species, adults participate animals are thought to have some type of intestine and termite hindgut, while oth- directly in the microbial colonization of symbiotic prokaryote living inside them, ers have actually invaded host cells and juveniles: Adult termite workers feed their although these relationships can span a live almost as organelles. A few animals, feces to newly hatched juveniles, pre- vast continuum from fleeting to requisite including deep-sea shrimp and nema- sumably to ensure the juveniles’ hindguts and from beneficial to pathogenic. todes that live in coastal sediments, pos- are exposed to the correct consortia of Prokaryotes can influence host biology sess permanent bacterial coats on the bacteria. and evolution in incredibly diverse ways. outside of their bodies. A host’s reliance on its symbionts also Luminescent bacteria form light organs The site of colonization in the host spans a wide spectrum, from pathogens in many species of fish, possibly for dif- tends to correlate—although not that the host’s body actively tries to elim- ferent evolutionary reasons. Bacteria absolutely—with how the symbiont is inate to obligate symbionts, without called Wolbachia are reproductive para- transmitted from generation to genera- which the host dies. Insects that feed ex- sites in insects but obligate mutualists in tion. Intracellular symbionts are fre- clusively on restricted diets, such as plant nematodes. Beetles’ symbionts secrete a quently passed vertically from mother sap, blood, or wood, often receive essen- 376 BioScience • May 2006 / Vol. 56 No. 5 www.biosciencemag.org Feature tial nutrients from their symbiotic part- ners and cannot reproduce without them. Many animals also possess an array of fac- ultative symbionts, whose composition may change frequently. Relationships are obligate or facultative from the symbionts’ point of view, as well: Vertically transmitted bacteria that provision their hosts with essential nu- trients often have such degraded genomes that they could not hope to survive out- side a host. Many horizontally transmit- Downloaded from https://academic.oup.com/bioscience/article/56/5/376/234704 by guest on 01 October 2021 ted symbionts, however, have a free-living stage in which they fend for themselves. The Hawaiian bobtail squid, Euprymna scolopes, contains a light organ Biologists have often been reluctant filled with luminescent bacteria called Vibrio fischeri. The squid–Vibrio to consider how such associations have af- relationship is one of the best-studied animal–bacterial symbioses. fected the evolution and development of Photograph: Margaret McFall-Ngai, University of Wisconsin–Madison. the animals they study, says McFall-Ngai. “On occasion, they will think about how environmental pressure will influence other, and scientists have developed ex- host gene expression that alter the mor- development, and they think about tem- perimental genetic systems in both or- phology of the light organ. Bacterial mor- perature and pressure and osmolarity,” ganisms that permit control over genes of phology and gene expression also change says McFall-Ngai. “Rarely do they think interest. upon establishment of the symbiosis. about biotic pressure.” A similar swap of genetic messages The symbionts alter their surface com- This neglect stems at least somewhat appears to occur in one of the most ponents and the signal molecules they from technological difficulties in study- successful models of animal–bacterial export, both of which encourage the sym- ing microorganisms. Laboratory cultures symbiosis: the association between the biosis to move forward. are difficult for many free-living bacteria Hawaiian bobtail squid, Euprymna Molecular genetic manipulation of V. and most likely impossible for those scolopes, and its luminescent bacterial fischeri has allowed scientists to find bac- living completely dependent existences symbiont, Vibrio fischeri.The V. fischeri terial genes required to establish, pro- inside animals. But new and improving live inside the squid’s light organ and mote, and maintain the symbiosis, technologies, especially in high-throughput emit light of the same color and intensity McFall-Ngai says. She and others are now DNA sequencing and genomics, are al- as moonlight and starlight, thereby pre- working on techniques involving anti- lowing biologists to survey symbiotic in- venting the nocturnal squid from casting sense probes and viral vectors to knock teractions as never before. a dark shadow visible to predators or down expression of certain genes in the prey below. squid to see how that affects symbiosis de- Experimenting with symbioses Like the legume–rhizobium sym- velopment. Much of what is known about symbioses biosis, the squid–vibrio symbiosis is Another animal system that promises between prokaryotes and eukaryotes binary—one symbiont, one host. And, to reveal more about the development of comes from the study of leguminous although Euprymna normally become animal–bacterial symbioses is the germ- plants and a group of nitrogen-fixing colonized with free-living V. fischeri free mouse model. Observations of mice bacteria called rhizobia. These bacteria fix within minutes to hours after they hatch raised in sterile environments can reveal atmospheric nitrogen for the host plant as juveniles, they can be kept sterile past how the microbial community as a whole in exchange for carbon and protected this stage in the lab and later infected contributes to mammalian development housing in the plant’s root nodules. These at various ages. Such experiments have and physiology. Adding one or a few nodules develop over weeks of back-and- revealed much about how these part- members of the normal gut microbiota forth gene expression between plant and ners interact and influence each other’s back into a germ-free mouse’s gastro- bacterium, creating a conversation that biology. intestinal tract can also elucidate those begins with each partner recognizing the During embryogenesis, developing microorganisms’ specific roles in the other and results in the morphogenesis of squid acquire a ciliated tissue whose sole community. the root nodule. purpose appears to be to promote later Beginning at birth, mammals amass Legume–rhizobium symbioses have bacterial colonization. Squid mothers incredibly complex microbial consortia made ideal experimental models for sev- lay their eggs in areas enriched for V. in many body regions, especially in the in- eral reasons, says McFall-Ngai: They in- fischeri, and after symbionts colonize the testine. A human gut, for example, carries volve only one host and one symbiont, hatchlings, both partners undergo major up to a thousand species of mainly anaer- both partners can be cultured without the changes. The bacteria induce changes in obic microorganisms, which together en- www.biosciencemag.org May 2006 / Vol. 56 No. 5 • BioScience 377 Feature compass about 10 times as many cells as sess obligate intracellular symbionts that are in the entire human body. provide the host with essential nutrients. Mammals’ relationship with intesti- These “primary” symbionts live inside nal microbiota was probably driven by a specialized host cells called bacteriocytes, nutritional need, just as in the vast ma- which make up a dedicated organ in the jority of animal–bacterial symbioses, says anterior gut, called the bacteriome. Many Lora Hooper, a molecular biologist at of these insects also have “secondary” the University of Texas Southwestern symbionts that live outside the bacteri- Medical Center in Dallas. ome. A well-established example of this Ribosomal RNA analyses in sap- symbiosis is found in ruminants like feeding aphids and their primary sym- Downloaded from https://academic.oup.com/bioscience/article/56/5/376/234704 by guest on 01 October 2021 cows, sheep, and deer. These animals biont Buchnera aphidicola have shown are able to digest grass because bacteria that Buchnera infected an ancestor of all of today’s aphids between 200 and
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