Deciphering the genomic toolkit underlying animal-bacteria interactions – insights through the demosponge Amphimedon queenslandica

Abstract

All animals are inhabited by bacteria, and maintaining homeostasis in the multicellular environment of the host involves the complex balancing act of promoting the survival of symbionts while defending against intruders. Sponges (Porifera), in addition to housing diverse bacterial symbiont assemblages, also rely on bacteria filtered from the water column for nutrition. My research uses the genome-enabled demosponge, Amphimedon queenslandica, a member of one of the earliest-diverging animal phyletic lineages, as an experimental platform to investigate the genomic toolkit underpinning animal-bacteria interactions. Using comparative bioinformatics tools, I characterised a surprisingly large and complex repertoire of innate immune receptors from the NLR family of genes encoded in the A. queenslandica genome. I then used a high throughput RNAseq approach to profile the sponge's global transcriptomic response to foreign versus its own native bacteria. Conserved metazoan innate immune pathways were activated in response to both foreign and native bacteria. However, only the native bacteria elicited the expression of a more extensive suite of signalling pathways, involving TGF-β signalling and the transcription factors NF-κB and FoxO. Upregulation of the nutrient sensor AMPK in all treatments along with immune signalling genes, which all regulate FoxO activity, further suggests an interplay between metabolic homeostasis and immunity. Finally, I used microscopy to track the cellular-level processing of the different bacteria by the sponge. Consistent with the observed transcriptional response, the native bacteria were ingested by archaeocytes more rapidly than the foreign bacteria. The slower processing of foreign bacteria also correlated with the expression of numerous Nrf2-associated detoxification genes, indicative of cellular stress, only in response to foreign bacteria.iii Deciphering the genomic tool-kit underlying animal-bacteria interactions

Origin and evolution of the metazoan non-coding regulatory genome: Insights from the sponge Amphimedon queenslandica

“…Consistent with this premise, these three lncRNAs were found to be DE when Amphimedon juveniles were exposed to a foreign bacterial suspension enriched from a different sponge species (Rhabdastrella globostellata, Carter 1883) (Yuen, 2016). Moreover, this finding runs parallel to SRCR genes being upregulated in choanocytes (Yuen, 2016) and is consistent with the proposed dual role of this cell type in sponge digestion (Mah et al, 2014) and immunity (Yuen, 2016).…”

Exploring the bZIP regulatory network in the sponge Amphimedon queenslandica: insights into the ancestral animal regulatory genome

“…Recognition of non-symbiotic bacteria is of prime importance and is thought to be achieved though the NRF2 pathway (Yuen, 2016). Notably, differential expression of AqNFE2s in juvenile under bacterial infection strongly supports this hypothesis (Yuen, 2016). Consistent with this idea, the AqNFE2a expression profile correlates with that of a suite of genes associated with cellular response to stress.…”

“…Sponges rely on the phagocytosis of a variety of particles, notably free-living bacteria, by choanocytes for feeding and they maintain a bacteria symbiont. Recognition of non-symbiotic bacteria is of prime importance and is thought to be achieved though the NRF2 pathway (Yuen, 2016). Notably, differential expression of AqNFE2s in juvenile under bacterial infection strongly supports this hypothesis (Yuen, 2016).…”

“…Both the NFE2 and PAR bZIP families are metazoan-specific (Chapter 2). Interestingly, A. queenslandica NFE2 bZIPs and canonical members of the Nrf2 pathway are upregulated in juveniles under bacterial infection (Yuen, 2016), suggesting that the involvement of NFE2 bZIPs in immune response dates back to the animal last common ancestor (LCA). Similarly, one of A. queenslandica PAR-bZIP is involved in this sponge circadian-like response to light (Chapter 4).…”

The biology of choanocytes and choanocyte chambers and their role in the sponge stem cell system

“…In A. queenslandica, the uptake and subsequent transfer of food particles occurs fairly quickly, with fluorescently labeled bacteria found in mesohyl cells around choanocyte chambers within 2-8 hours (Yuen, 2016 PhD thesis). However, this observation was based on tracking the location of fluorescently labeled bacteria, and did not observe cell movement per se.…”