Sea Slug—Algal Chloroplast Symbiosis: Towards an Integrated Understanding of Long-Term Chloroplast Functioning in an Animal

Photosynthesis plays a fundamental role in understanding plant growth and productivity. The chloroplast, the organelle of photosynthesis, evolved following the endosymbiotic uptake of a cyanobacterium and massive gene transfer. As a result, the chloroplast is highly dependent upon nuclear genes to provide essential chloroplast proteins. A special form of endosymbiosis, kleptoplasty, has evolved in the marine mollusc Elysia chlorotica. This green, leaf-like animal carries out photosynthesis for its entire ten month life-cycle, as if it were a plant, by using chloroplasts it steals and retains from the alga Vaucheria litorea. It is highly likely that horizontal gene transfer (HGT) has occurred between these two unrelated multi-cellular organisms, to support the long-term activity of the chloroplasts in the sea slug. The overall approach of this study is to combine cellular and molecular analyses with studies of whole animal biology to understand how such an endosymbiotic association can form and be sustained, and also influence the evolution of photosynthesis in an animal. These studies will identify specific examples of HGT from the alga to the sea slug, where and how the genes are integrated into the animal DNA, the mechanism of recognition and uptake of the chloroplasts, and the specificity of the association. The broader impact of these studies is seen at many levels. Fascinating organisms can transform the teaching of basic principles in biology; hence, the solar-powered sea slugs will be exploited in developing multimedia educational materials for students of all ages. Kleptoplastic sea slugs also potentially have a direct bearing on human health, through their production of anti-cancer compounds. The ability to culture the sea slugs will provide a supply of this unusual organism for classrooms and laboratories, marine hobbyists, and contributes to protection of a rare species and its native habitat

Biochemical and Molecular Autonomy of Symbiotic Chloroplasts

Photosynthesis provides the energy that drives all plant growth, productivity and life on earth. A marine sea slug, Elysia chlorotica, has acquired the ability to carry out photosynthesis like a plant as a result of forming a symbiotic association with chloroplasts of the alga, Vaucheria litorea. Juvenile sea slugs feed on the filamentous alga and retain only the chloroplasts, incorporating them into cells of the digestive epithelium. The chloroplasts in the now dark-green animals are functional, i.e. they evolve oxygen and fix carbon dioxide and actively synthesize proteins from DNA contained in the chloroplasts. Once the symbiosis is established, the animal can live and reproduce in culture without eating for the rest of its normal life span of nine to ten months. About 90% of all the proteins required to keep chloroplasts functioning and carrying out photosynthesis are encoded by DNA in the nucleus of the plant or alga. These proteins must be continually synthesized in the cell and transported into the chloroplast to sustain activity. Thus, considering that the sea slugs only acquire the algal chloroplasts and not any other part of the algal cell including the nucleus, the level of sustained chloroplast activity observed in the sea slugs is unique and quite remarkable.Understanding how these chloroplasts are able to remain photosynthetically active outside of their normal cellular environment for months when higher plant chloroplasts survive only a few hours in isolation, forms the basis of the specific objectives of this proposal. These include: 1) Characterizing the structural and functional long-term stability of isolated plastids, the stability of plastid proteins, and the activity of chloroplast proteases in sea slugs vs. algae, 2) Determining if the sea slug nuclear genome codes for and targets any proteins to the symbiotic chloroplasts and elucidating the general mechanism of protein import in chloroplasts, and 3) Characterizing the genetic autonomy of the chloroplasts by mapping and sequencing the chloroplast genome of the alga.This symbiotic organism provides a unique opportunity to determine how the chloroplasts from one organism (alga) can form a long-term functional photosynthetic union with the cell of an extremely divergent organism (sea slug). This represents a process molecular data indicate occurred repeatedly over evolutionary history resulting in the diversity of plants and algae on earth today. On a much broader scale, this project possibly represents lateral gene transfer between two diverse organisms and endosymbiosis in action. The Solar-Powered Sea Slugs are a fascinating teaching tool eliciting excitement and curiosity from people all around the world from scientists of several disciplines to graduate and undergraduate students discovering them in their readings in journal clubs, to young children who have seen these crawling leaves on the Internet or researched them for science fair projects. The endosymbiotic theory has generated and continues to generate much interest at all levels, but to actually observe a symbiotic association in a potentially evolving situation and imparting such a major new function to the other partner, is indeed rare and a unique opportunity for study

Active host response to algal symbionts in the sea slug Elysia chlorotica

Sacoglossan sea slugs offer fascinating systems to study the onset and persistence of algal-plastid symbioses. Elysia chlorotica is particularly noteworthy because it can survive for months, relying solely on energy produced by ingested plastids of the stramenopile alga Vaucheria litorea that are sequestered in cells lining its digestive diverticula. How this animal can maintain the actively photosynthesizing organelles without replenishment of proteins from the lost algal nucleus remains unknown. Here we used RNA-Seq analysis to test the idea that plastid sequestration leaves a significant signature on host gene expression during E. chlorotica development. Our results support this hypothesis and show that upon exposure to and ingestion of V. litorea plastids, genes involved in microbe-associated molecular patterns (MAMPs) and oxidative stress-response mechanisms are significantly up-regulated. Interestingly, our results with E. chlorotica mirror those found with corals that maintain dinoflagellates as intact cells in symbiosomes, suggesting parallels between these animal-algal symbiotic interactions

The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing

International audienceCurrent sampling of genomic sequence data from eukaryotes is relatively poor, biased, and inadequate to address important questions about their biology, evolution, and ecology; this Community Page describes a resource of 700 transcriptomes from marine microbial eukaryotes to help understand their role in the world's oceans

The rhizosphere microbiota of plant invaders: an overview of recent advances in the microbiomics of invasive plants

Plants in terrestrial systems have evolved in direct association with microbes functioning as both agonists and antagonists of plant fitness and adaptability. As such, investigations that segregate plants and microbes provide only a limited scope of the biotic interactions that dictate plant community structure and composition in natural systems. Invasive plants provide an excellent working model to compare and contrast the effects of microbial communities associated with natural plant populations on plant fitness, adaptation, and fecundity. The last decade of DNA sequencing technology advancements opened the door to microbial community analysis, which has led to an increased awareness of the importance of an organism’s microbiome and the disease states associated with microbiome shifts. Employing microbiome analysis to study the symbiotic networks associated with invasive plants will help us to understand what microorganisms contribute to plant fitness in natural systems, how different soil microbial communities impact plant fitness and adaptability, specificity of host-microbe interactions in natural plant populations, and the selective pressures that dictate the structure of above-ground and below-ground biotic communities. This review discusses recent advances in invasive plant biology that have resulted from microbiome analyses as well as the microbial factors that direct plant fitness and adaptability in natural systems