Final Report Summary - COSMIC (COral Surface MICrolayer: production and dynamics of mucus-associated microbial communities)
Mucus mediates the interaction of most animals with their surrounding environment as well as with other organisms. In fact, mucus plays also a major role in the immunity system of animals, such as we humans experience when we catch a cold. Another such example is the human intestinal mucus, which provides a nutrient- and niche-rich ecosystem for many symbiotic microorganisms. These microorganisms are beneficial to its host and keep away potential pathogens, thereby supporting its health and well-being. Shifts in the composition of these microbial communities are often associated with the occurrence of host diseases.
A way to understand host-microbial interactions in mucus interfaces is to study the most primordial animals that secrete mucus. In fact, the mucosa is an evolutionary novelty in the phylum Cnidaria, to which corals belong. Corals, small anemone-like animals that form colonies, have the amazing capacity to build iconic and colorful reefs and offer an interesting model system to study the microbial life in mucus layers. Coral surface mucus is responsible for important biological functions of the host (sediment cleansing, particulate feeding), and provides an interface between the coral and the surrounding environment. Being formed by a complex mixture of proteins, lipids and sugars, coral mucus is a source of nutrients for microbial growth and offers a habitat for a diverse consortium of microorganisms. The main goal of COSMIC was to understand the dynamics in the composition of the coral surface mucus layer, in its secretion and release and the related changes in the structure and abundance of its associated microbial community. The project is now completed and accomplished all the proposed objectives: 1) To determine the natural variation of the thickness, chemical properties and release of coral mucus in different coral species and to define distinct types of mucus microenvironments. 2) To compare the phylogenetic structure of the mucus-associated microbial community and the relative abundance of its constituents in common coral species over a depth gradient. 3) To analyze the specificity of microbial assemblages of coral mucus by comparing distinct coral species to the microbiome present in the surrounding water and sediment. 4) To understand the dynamics of adherence, establishment and temporal succession of microbial assemblages within freshly released coral mucus. 5) To elucidate the functional potential of coral mucus microbes and identify (unique) metabolic pathways and adaptations associated with the coral holobiont.
One main finding is that coral surface mucus layer shows interspecific variation in physical and chemical parameters, offering what we interpret as a wide range of niches for microbial propagation. This microscale heterogeneity within the mucus layer suggests that potentially different metabolic processes are taking place in the mucus of distinct corals. We hypothesize that microbial taxa with distinct lifestyles may occupy different positions within the mucus layer.
A surprising pattern arose when looking at carbohydrate composition of coral mucus. Coral species can be split into broad phylogenetic groups depending on the main carbohydrate of their mucus: either fucose, galactose or mannose. Interestingly, the dominant carbohydrate in the mucus seems to correlate to the composition of the microbial community inhabiting this mucus layer. This constitutes a mechanism to be further explored, potentially explaining the host-specificity of the associated microbial biofilms. Results also point to substantial differences in the community structure between Bacteria and Archaea. While the bacterial community composition was determined by habitat, host coral species, location and spatial distance, the archaeal community composition was solely determined by the habitat. This study highlights that mucus-associated archaeal and bacterial communities differ in their degree of community turnover over reefs and in their host-specificity, suggesting that these two groups constitute distinct ecological guilds within the coral holobiont.
Another main finding was that the natural microbial communities inhabiting coral mucus crucially contribute to coral health by presenting cyclical oscillations that relate to behavioural mechanisms of the host. In particular, the typical coral behaviour of shedding a conspicuous thickened and hardened mucus sheet after a period of mucus ageing constitutes a defense mechanism allowing the coral to maintain beneficial microbes while getting rid of unwanted microbes such as pathogens. This study supports the view that the natural prokaryotic community inhabiting coral mucus crucially contributes to coral health and hence, to coral reef resilience.
COSMIC was also the first study providing a quantification of the bacteria involved in the degradation of sulphur compounds produced by corals and to link related changes in the community dynamics of these bacteria to sulphur availability. Our findings suggest that sulphur mediates the interplay between corals and microbes, highlighting the importance of sulfur compounds for microbial processes in corals and for the resilience of coral reef ecosystems.
The COSMIC project will contribute to a better understanding of the relationships established between corals and microbes in particular, and between animal hosts and their associated microbes in general, potentially contributing to further extrapolations relevant for biomedical research and the fields of human immunity and nutrient complementation by human microbiome.
A way to understand host-microbial interactions in mucus interfaces is to study the most primordial animals that secrete mucus. In fact, the mucosa is an evolutionary novelty in the phylum Cnidaria, to which corals belong. Corals, small anemone-like animals that form colonies, have the amazing capacity to build iconic and colorful reefs and offer an interesting model system to study the microbial life in mucus layers. Coral surface mucus is responsible for important biological functions of the host (sediment cleansing, particulate feeding), and provides an interface between the coral and the surrounding environment. Being formed by a complex mixture of proteins, lipids and sugars, coral mucus is a source of nutrients for microbial growth and offers a habitat for a diverse consortium of microorganisms. The main goal of COSMIC was to understand the dynamics in the composition of the coral surface mucus layer, in its secretion and release and the related changes in the structure and abundance of its associated microbial community. The project is now completed and accomplished all the proposed objectives: 1) To determine the natural variation of the thickness, chemical properties and release of coral mucus in different coral species and to define distinct types of mucus microenvironments. 2) To compare the phylogenetic structure of the mucus-associated microbial community and the relative abundance of its constituents in common coral species over a depth gradient. 3) To analyze the specificity of microbial assemblages of coral mucus by comparing distinct coral species to the microbiome present in the surrounding water and sediment. 4) To understand the dynamics of adherence, establishment and temporal succession of microbial assemblages within freshly released coral mucus. 5) To elucidate the functional potential of coral mucus microbes and identify (unique) metabolic pathways and adaptations associated with the coral holobiont.
One main finding is that coral surface mucus layer shows interspecific variation in physical and chemical parameters, offering what we interpret as a wide range of niches for microbial propagation. This microscale heterogeneity within the mucus layer suggests that potentially different metabolic processes are taking place in the mucus of distinct corals. We hypothesize that microbial taxa with distinct lifestyles may occupy different positions within the mucus layer.
A surprising pattern arose when looking at carbohydrate composition of coral mucus. Coral species can be split into broad phylogenetic groups depending on the main carbohydrate of their mucus: either fucose, galactose or mannose. Interestingly, the dominant carbohydrate in the mucus seems to correlate to the composition of the microbial community inhabiting this mucus layer. This constitutes a mechanism to be further explored, potentially explaining the host-specificity of the associated microbial biofilms. Results also point to substantial differences in the community structure between Bacteria and Archaea. While the bacterial community composition was determined by habitat, host coral species, location and spatial distance, the archaeal community composition was solely determined by the habitat. This study highlights that mucus-associated archaeal and bacterial communities differ in their degree of community turnover over reefs and in their host-specificity, suggesting that these two groups constitute distinct ecological guilds within the coral holobiont.
Another main finding was that the natural microbial communities inhabiting coral mucus crucially contribute to coral health by presenting cyclical oscillations that relate to behavioural mechanisms of the host. In particular, the typical coral behaviour of shedding a conspicuous thickened and hardened mucus sheet after a period of mucus ageing constitutes a defense mechanism allowing the coral to maintain beneficial microbes while getting rid of unwanted microbes such as pathogens. This study supports the view that the natural prokaryotic community inhabiting coral mucus crucially contributes to coral health and hence, to coral reef resilience.
COSMIC was also the first study providing a quantification of the bacteria involved in the degradation of sulphur compounds produced by corals and to link related changes in the community dynamics of these bacteria to sulphur availability. Our findings suggest that sulphur mediates the interplay between corals and microbes, highlighting the importance of sulfur compounds for microbial processes in corals and for the resilience of coral reef ecosystems.
The COSMIC project will contribute to a better understanding of the relationships established between corals and microbes in particular, and between animal hosts and their associated microbes in general, potentially contributing to further extrapolations relevant for biomedical research and the fields of human immunity and nutrient complementation by human microbiome.