Secondary Metabolite Production Potential in a Microbiome of the Freshwater Sponge Spongilla lacustris

Author(s)
Sophie Graffius, Jaime Felipe Guerrero Garzón, Martin Zehl, Petra Pjevac, Rasmus Kirkegaard, Mathias Flieder, Alexander Loy, Thomas Rattei, Andrew Ostrovsky, Sergey B Zotchev
Abstract

Marine and freshwater sponges harbor diverse communities of bacteria with vast potential to produce secondary metabolites that may play an important role in protecting the host from predators and infections. In this work, we initially used cultivation and metagenomics to investigate the microbial community of the freshwater sponge Spongilla lacustris collected in an Austrian lake. Representatives of 41 bacterial genera were isolated from the sponge sample and classified according to their 16S rRNA gene sequences. The genomes of 33 representative isolates and the 20 recovered metagenome-assembled genomes (MAGs) contained in total 306 secondary metabolite biosynthesis gene clusters (BGCs). Comparative 16S rRNA gene and genome analyses showed very little taxon overlap between the recovered isolates and the sponge community as revealed by cultivation-independent methods. Both culture-independent and -dependent analyses suggested high biosynthetic potential of the S. lacustris microbiome, which was confirmed experimentally even at the subspecies level for two

Streptomyces isolates. To our knowledge, this is the most thorough description of the secondary metabolite production potential of a freshwater sponge microbiome to date.

IMPORTANCE A large body of research is dedicated to marine sponges, filter-feeding animals harboring rich bacterial microbiomes believed to play an important role in protecting the host from predators and infections. Freshwater sponges have received so far much less attention with respect to their microbiomes, members of which may produce bioactive secondary metabolites with potential to be developed into drugs to treat a variety of diseases. In this work, we investigated the potential of bacteria associated with the freshwater sponge

Spongilla lacustris to biosynthesize diverse secondary metabolites. Using culture-dependent and -independent methods, we discovered over 300 biosynthetic gene clusters in sponge-associated bacteria and proved production of several compounds by selected isolates using genome mining. Our results illustrate the importance of a complex approach when dealing with microbiomes of multicellular organisms that may contain producers of medically important secondary metabolites.

Organisation(s)
Department of Pharmaceutical Sciences, Mass Spectrometry Centre, Department of Analytical Chemistry, Department of Microbiology and Ecosystem Science, Research Platform Secondary metabolomes of bacterial communities, Department of Palaeontology
External organisation(s)
Medizinische Universität Wien
Journal
Microbiology Spectrum
Volume
11
ISSN
2165-0497
DOI
https://doi.org/10.1128/spectrum.04353-22
Publication date
02-2023
Peer reviewed
Yes
Austrian Fields of Science 2012
106014 Genomics, 104013 Natural product chemistry, 106022 Microbiology
Keywords
ASJC Scopus subject areas
Microbiology (medical), Infectious Diseases, Genetics, General Immunology and Microbiology, Physiology, Cell Biology, Ecology
Sustainable Development Goals
SDG 14 - Life Below Water
Portal url
https://ucrisportal.univie.ac.at/en/publications/bd21ae8f-c8bd-46ac-9dc4-d5642b041e67