Microbiome exploration of deep-sea carnivorous Cladorhizidae sponges

Verhoeven, Joost T. P. (2019) Microbiome exploration of deep-sea carnivorous Cladorhizidae sponges. Doctoral (PhD) thesis, Memorial University of Newfoundland.

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Abstract

Members of the sponge family Cladorhizidae are unique in having replaced the typical filter-feeding strategy of sponges by a predatory lifestyle, capturing and digesting small prey. These carnivorous sponges are found in many different environments, but are particularly abundant in deep waters, where they constitute a substantial component of the benthos. Sponges are known to host a wide range of microbial associates (microbiome) important for host health, but the extent of the microbiome in carnivorous sponges has never been extensively investigated and their importance is poorly understood. In this thesis, the microbiome of two deep-sea carnivorous sponge species (Chondrocladia grandis and Cladorhiza oxeata) is investigated for the first time, leveraging recent advances in high-throughput sequencing and through custom developed bioinformatic and molecular methods. Microbiome analyses showed that the carnivorous sponges co-occur with microorganisms and large differences in the composition and type of associations were observed between sponge species. Tissues of C. grandis hosted diverse bacterial communities, similar in composition between individuals, in stark contrast to C. oxeata where low microbial diversity was found with a high host-to-host variability. In C. grandis the microbiome was not homogeneous throughout the host tissue, and significant shifts occured within community members across anatomical regions, with the enrichment of specific bacterial taxa in particular anatomical niches, indicating a potential symbiotic role of such taxa within processes like prey digestion and chemolithoautotrophy. The potential for bacteria-mediated chemolithoautotrophy was further supported by stable-isotope analysis in C. grandis but not in C. oxeata. Metagenome analysis further showed a potential role for archaea in nitrogenous-waste detoxification, as well as an assemblage of bacteriophages potentially influencing the bacterial community composition and functionality. Lastly, metabolic pathways of associated microbes were diverse and included metabolism of elemental substrates (nitrogen, sulfur) and methane. This thesis provides novel insights into the role of microorganisms in carnivorous sponges and their relation to carnivory; the microbiome of C. grandis is linked to many metabolic functions, including the facilitation of carnivory, whereas heterogeneity and absence of apparent symbiotic potential in C. oxeata suggest that in some sponges, other processes govern carnivory.

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