Microbial diversity and function in sponge symbioses

Sponges (Porifera), representing one of the oldest, still living animal phyla, are multicellular organisms with various differentiated cell types. Many sponge species harbor enormously dense and diverse microbial communities in their tissues. Microbial representatives from several dozen bacterial phyla, among them many candidate lineages, two archaeal lineages, and an enormous viral diversity have been identified in association with these animals. In fact, microbial biomass can comprise up to one third of the total sponge biomass and is located extracellularly within the sponge extracellular matrix. Since sponge symbionts have resisted cultivation to this date, meta-omic approaches, in combination in combination with high-resolution microscopy (i.e., FISH-IHC-CLEM), have been instrumental to reveal the functions of the collective microbial community as well as of individual symbiont groups.

Symbiotic Heterotrophy

Our major finding is that many of the functional roles originally attributed to the sponge are indeed mediated by their associated microbes. These functions include complex and varied heterotrophic pathways allowing symbionts to utilize the nutrients either produced by the host itself or filtered in from the surrounding seawater (Dr. Kristina Bayer), pathways that contribute to the chemical defense of the animal and molecular signatures that enable symbiont persistence within the animal. While many symbioses are known for their nutritional basis based on phototrophic or chemoautotrophic metabolisms, our collective research efforts including that of our previous postdoc Dr. Laura Rix (University of Queensland) have brought marine heterotrophic symbioses to the front.

 

The role of phages in tripartite interplay

While recent studies have revealed vast diversity in the virosphere, the new frontier is to understand how phages modulate host-microbe interactions. We combine viral metagenomics with functional assays to investigate the interplay between phages, bacterial symbionts and marine sponges. Although sponges process massive amounts of water through their constantly operating filter apparatus, we have recently shown that they harbor species specific and even individually unique viral signatures distinct from other environments. We have further discovered an ankyrin protein (ANKp), encoded on a symbiont phage that, upon heterologous expression, modulates the eukaryotic immune response against bacteria as confirmed in macrophage infection assays. We hypothesize that these symbiont phage proteins facilitate co-existence in the multispecies interplay between phages, microbial symbionts and sponges in a manner that may extend to other host-microbe associations. Interestingly, these “Ankyphages” appear to be widely distributed in other host-associated contexts including human.

Researchers

Dr. Kristina Bayer, Dr. Beate Slaby, Dr. Martin Jahn (Oxford), Dr. Laura Rix (Queensland), Clara Emery,  Leon Steiner

Publications

Rix L, Ribes M, Coma R, Jahn M, van Oevelen D, de Goeij J, Escrig S, Meibom A, Hentschel U (2020) Heterotrophy in the earliest gut: A single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses. ISME J: doi.org/10.1038/s41396-020-0706-3

Jahn MT, Arkhipova K, Markert SM, Stigloher C, Lachnit T, Pita L, Kupczok A, Ribes M, Stengel ST, Rosenstiel P, Dutilh BE, Hentschel U(2019). A phage protein aids bacterial symbionts in eukaryote immune evasion.Cell Host & Microbe 26(4):542-550.e5. doi: 10.1016/j.chom.2019.08.019.

Batani G, Bayer K, Böge J, Hentschel  U, Thomas T (2019) Fluorescence in situ hybridization (FISH) and cell sorting of living bacteria.Sci Rep 9(1):18618. doi: 10.1038/s41598-019-55049-2.

Bayer K, Jahn MT, Slaby BM, Moitinho-Silva L, Hentschel U (2018) Marine sponges as Chloroflexi Hot Spots: Genomic insights and high resolution visualization of an abundant and diverse symbiotic clade. mSystems: doi.org/10.1128/mSystems.00150-18

Slaby BM, Hackl T, Horn H, Bayer K, Hentschel U (2017) Metagenomic binning of a marine sponge microbiome reveals unity in defense but metabolic specialization. ISME J. 11(11): 2465-2478. doi: 10.1038/ismej.2017.101.

Funding

SFB 1182/2: Origin and Function of Metaorganisms

http://www.metaorganism-research.com/