Periodic Reporting for period 4 - EvoLucin (400 Million Years of Symbiosis: Host-microbe interactions in marine lucinid clams from past to present)
Okres sprawozdawczy: 2023-08-01 do 2024-12-31
Virtually every animal on Earth evolved with and among trillions of microbes in the environment. Interactions with these microbes are mostly invisible to the human eye, thus, their wide-ranging effects were long overlooked in biology. The current ‘microbiome revolution’ is bringing widespread attention to the effects of microbes on almost every aspect of animal (including human) biology.
Despite this, we so far understand the underlying mechanisms in very few systems. This knowledge is the basis for manipulating microbiomes for better environmental, animal, and human health. There is still immense potential for discovering fundamentally new mechanisms of host-microbe interaction among the staggering diversity of animals and their microbial symbionts in nature. This project aims to use the ancient and exclusive association between marine lucinid clams and chemosynthetic symbiotic bacteria to investigate fundamental aspects of host-microbe interactions.
Lucinidae is one of the most widespread and species-rich animal families in the oceans today, and has lived in symbiosis for more than 400 million years. The clam’s outstanding ability to select one specific symbiont from the trillions of bacteria in its environment challenges widely held assumptions about the function and specificity of the innate immune system. Symbiont-free juveniles can be raised in the lab, and experimentally infected, allowing unmatched insights into the early development of this symbiosis. Although the symbiont infection is specific to gill cells, symbiont-encoded proteins can be found in distant parts of the animal that are symbiont-free. This project combines cutting-edge molecular tools and experimental infection to better understand three key aspects of host-microbe interactions in these clams: 1) Acquisition and selection of microbes during animal development, 2) Maintenance along animal lifetimes through molecular communication and exchange, and 3) Emergence and perpetuation over evolution. I hypothesize that intracellular bacterial symbionts fundamentally alter host biology, and these effects are not limited to the location where symbionts are housed, but can affect distant organ systems. The overarching goal is to understand the molecular basis for these effects, and their evolutionary history.
Despite this, we so far understand the underlying mechanisms in very few systems. This knowledge is the basis for manipulating microbiomes for better environmental, animal, and human health. There is still immense potential for discovering fundamentally new mechanisms of host-microbe interaction among the staggering diversity of animals and their microbial symbionts in nature. This project aims to use the ancient and exclusive association between marine lucinid clams and chemosynthetic symbiotic bacteria to investigate fundamental aspects of host-microbe interactions.
Lucinidae is one of the most widespread and species-rich animal families in the oceans today, and has lived in symbiosis for more than 400 million years. The clam’s outstanding ability to select one specific symbiont from the trillions of bacteria in its environment challenges widely held assumptions about the function and specificity of the innate immune system. Symbiont-free juveniles can be raised in the lab, and experimentally infected, allowing unmatched insights into the early development of this symbiosis. Although the symbiont infection is specific to gill cells, symbiont-encoded proteins can be found in distant parts of the animal that are symbiont-free. This project combines cutting-edge molecular tools and experimental infection to better understand three key aspects of host-microbe interactions in these clams: 1) Acquisition and selection of microbes during animal development, 2) Maintenance along animal lifetimes through molecular communication and exchange, and 3) Emergence and perpetuation over evolution. I hypothesize that intracellular bacterial symbionts fundamentally alter host biology, and these effects are not limited to the location where symbionts are housed, but can affect distant organ systems. The overarching goal is to understand the molecular basis for these effects, and their evolutionary history.
We were able to experimentally colonize juveniles of Codakia orbicularis to investigate the early establishment of symbiosis. Methods and protocols were developed to extract enough RNA and DNA from these, and from adult samples for any metagenomics or metatranscriptomic approaches. We discovered symbionts with identical 16S rRNA gene amplicon regions in lucinid clams and on seagrass roots at a location where both co-occur, revealing possible environmental symbiont reservoirs. We discovered that the 'gill' symbionts can colonize host cells throughout the host body, where they may have distinct functions in the symbiosis. Not only symbiont cells, but proteins synthesized by symbionts are also distributed throughout the body of the host, revealing a remarkable level of integration between the symbiotic partners over their long, shared, evolutionary history. We discovered symbionts with a panglobal distribution, and showed that nitrogen fixation genes tend to be lost during adaptation to particular habitats including deep-sea hydrothermal vents. At such extreme sites, we even discovered an unusual 'symbiont-switching' event, showing that this host family has the capacity to interact with symbionts outside the Sedimenticolaceae family of symbionts, an unexpected level of flexibility. Many of the results of the project are already published an available open access, many are currently in preparation for publication. The project team disseminated the results of the project at a range of national and international conferences. We established results and collaborations that may result in enabling lucinid clams to be used in industrial aquaculture settings in the future.
Our efforts brought us substantially closer to the goal of establishing a new experimental system for understanding fundamental aspects of host-microbe interactions. This system goes beyond the state of the art as it would be the first model of animal symbiosis where the symbionts invade the host cells from the environment.Host-microbe interactions are the basis for animal (including human) health and disease. A better understanding of the molecular underpinnings of these processes will help us to understand how these interactions function, and how they might have evolved. This understanding is of fundamental importance for a wide array of biological, environmental, and medical research fields.