Validation of key sponge symbiont pathways using genome‐centric metatranscriptomics

Author:

O'Brien Paul A.1234ORCID,Tan Shangjin5ORCID,Frade Pedro R.6ORCID,Robbins Steven J.4,Engelberts J. Pamela47ORCID,Bell Sara C.2,Vanwonterghem Inka4,Miller David J.89,Webster Nicole S.23410ORCID,Zhang Guojie1112ORCID,Bourne David G.123ORCID

Affiliation:

1. College of Science and Engineering, James Cook University Townsville Queensland Australia

2. Australian Institute of Marine Science Townsville Queensland Australia

3. AIMS@JCU Townsville Queensland Australia

4. Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland St Lucia Queensland Australia

5. BGI‐Shenzhen Beishan Industrial Zone Shenzhen China

6. Natural History Museum Vienna Vienna Austria

7. Centre for Microbiome Research Translational Research Institute, Queensland University of Technology Brisbane Queensland Australia

8. ARC Centre of Excellence for Coral Reef Studies, James Cook University Townsville Queensland Australia

9. Centre for Tropical Bioinformatics and Molecular Biology, James Cook University Townsville Queensland Australia

10. Australian Antarctic Division, Department of Climate Change Energy, Environment and Water Kingston Tasmania Australia

11. Centre for Evolutionary & Organismal Biology and Women's Hospital Zhejiang University, School of Medicine Hangzhou China

12. Liangzhu Laboratory Zhejiang University Medical Center Hangzhou China

Abstract

AbstractThe sponge microbiome underpins host function through provision and recycling of essential nutrients in a nutrient poor environment. Genomic data suggest that carbohydrate degradation, carbon fixation, nitrogen metabolism, sulphur metabolism and supplementation of B‐vitamins are central microbial functions. However, validation beyond the genomic potential of sponge symbiont pathways is rarely explored. To evaluate metagenomic predictions, we sequenced the metagenomes and metatranscriptomes of three common coral reef sponges: Ircinia ramosa, Ircinia microconulosa and Phyllospongia foliascens. Multiple carbohydrate active enzymes were expressed by Poribacteria, Bacteroidota and Cyanobacteria symbionts, suggesting these lineages have a central role in assimilating dissolved organic matter. Expression of entire pathways for carbon fixation and multiple sulphur compound transformations were observed in all sponges. Gene expression for anaerobic nitrogen metabolism (denitrification and nitrate reduction) were more common than aerobic metabolism (nitrification), where only the I. ramosa microbiome expressed the nitrification pathway. Finally, while expression of the biosynthetic pathways for B‐vitamins was common, the expression of additional transporter genes was far more limited. Overall, we highlight consistencies and disparities between metagenomic and metatranscriptomic results when inferring microbial activity, while uncovering new microbial taxa that contribute to the health of their sponge host via nutrient exchange.

Funder

Beijing Genomics Institute

Earthwatch Institute

Mitsubishi International Corporation

Publisher

Wiley

Subject

Ecology, Evolution, Behavior and Systematics,Microbiology

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