Localized production of defence chemicals by intracellular symbionts of Haliclona sponges

Abstract

Marine sponges often house small molecule producing symbionts extracellularly in their mesohyl, providing the host with means of chemical defense against predation and microbial infection. Here, we report an intriguing case of chemically mediated symbiosis between the renieramycin-containing sponge Haliclona sp. and its herein discovered renieramycin producing symbiont Candidatus Endohaliclona renieramycinifaciens. Remarkably, Ca . E. renieramycinifaciens has undergone extreme genome reduction where it has lost almost all necessary elements for free living while maintaining a complex, multi-copy-plasmid encoded biosynthetic gene cluster for renieramycin biosynthesis. In return, the sponge houses Ca . E. renieramycinifaciens in previously uncharacterized cellular reservoirs (chemobacteriocytes), where it can acquire nutrients from the host and avoid bacterial competition. This relationship is highly specific to a single clade of Haliclona sponges. Our study reveals intracellular symbionts as an understudied source for defense chemicals in the oldest living metazoans, and paves the way towards discovering similar systems in other marine sponges.

A multiproducer microbiome generates chemical diversity in the marine sponge Mycale hentscheli

“…Here, we reveal a contrasting scenario in which the source of three distinct cytotoxin families, the mycalamides (25), pateamines (27), and pelorusides (29), is a complex chemistry-based symbiosis in the poecilosclerid sponge M. hentscheli. Rather than production being localized in individual bacteria within BGC-depleted microbiomes (10,14,48), the data support a producer consortium in which multiple phylogenetically diverse members contribute to the overall rich chemistry of the holobiont. Other than BGCs assigned to the three known polyketide classes, this microbiome was found to contain numerous additional loci from distinct natural product families.…”

“…The bins with a >90% estimated genome completeness were analyzed for the presence of central metabolism and amino acid biosynthesis pathways (SI Appendix, Table S6). Although some of these pathways are partially or completely absent in some bins, we did not observe any cases of extreme genome reduction as found for various intracellular symbionts (48,49). Furthermore, we analyzed these bins for the presence of clusters of orthologous genes associated with symbiosis (SI Appendix, Table S7).…”

“…Among the latter is the provision of bioactive natural products that can be present as rich arrays in some holobionts (70). Such studies have identified single members within more diverse microbiomes that generate some or all of the specialized metabolites known from the host (10,14,20,48). Here, we reveal a contrasting scenario in which the source of three distinct cytotoxin families, the mycalamides (25), pateamines (27), and pelorusides (29), is a complex chemistry-based symbiosis in the poecilosclerid sponge M. hentscheli.…”

Quorum Sensing Signaling Alters Virulence Potential and Population Dynamics in Complex Microbiome-Host Interactomes

“…Adopting community-like behaviors through QS systems may offer a distinct competitive advantage as bacteria can attach to a form a biofilm like structure within the environment of the sponge. Community-based small molecular interactions may also be important with respect to intracellular sponge symbionts, such as the recently reported Candidatus Endohaliclona renieramycinifaciens intracellular interaction with Haliclona (Tianero et al, 2019).…”

Pseudopuniceibacterium antarcticum sp. nov., isolated from an Antarctic marine sponge

“…[4][5][6]). Most symbionts or microorganisms associated with marine sponges are as-yet uncultured, and are considered as rich sources of novel species and novel producers of bioactive compounds [2,3]. Indeed, around 40 novel species/ genera have been identified from sponges, and published in the International Journal of Systematic and Evolutionary Microbiology.…”