A diverse host thrombospondin-type-1 repeat protein repertoire promotes symbiont colonization during establishment of cnidarian-dinoflagellate symbiosis

Abstract

The mutualistic endosymbiosis between cnidarians and dinoflagellates is mediated by complex inter-partner signaling events, where the host cnidarian innate immune system plays a crucial role in recognition and regulation of symbionts. To date, little is known about the diversity of thrombospondin-type-1 repeat (TSR) domain proteins in basal metazoans or their potential role in regulation of cnidarian-dinoflagellate mutualisms. We reveal a large and diverse repertoire of TSR proteins in seven anthozoan species, and show that in the model sea anemone Aiptasia pallida the TSR domain promotes colonization of the host by the symbiotic dinoflagellate Symbiodinium minutum. Blocking TSR domains led to decreased colonization success, while adding exogenous TSRs resulted in a ‘super colonization’. Furthermore, gene expression of TSR proteins was highest at early time-points during symbiosis establishment. Our work characterizes the diversity of cnidarian TSR proteins and provides evidence that these proteins play an important role in the establishment of cnidarian-dinoflagellate symbiosis.DOI: http://dx.doi.org/10.7554/eLife.24494.001

Molecular signatures of host specificity linked to habitat specialization in Exaiptasia sea anemones

“…Both thrombospondin‐type‐1 repeat domain‐containing proteins (Neubauer et al., 2017) and genes involved in activating the complement system (Poole, Kitchen, & Weis, 2016) were more likely than expected by chance to exhibit strong associations with PC1 after correcting for multiple comparisons ( p =  .01 and p  =   .04, respectively; Table 4). We observed no evidence in our dataset indicating overall enrichment of SNPs strongly associated with PC1 in scavenger receptors ( p  =   .31; Neubauer et al., 2016) or genes differentially regulated during symbiosis establishment in larvae ( p =  .52; Wolfowicz et al., 2016).…”

“…Loci in several TSR domain genes were also highly differentiated. In a previous study, blocking TSR domains decreased colonization of Exaiptasia anemones by symbionts, whereas addition of exogenous TSRs resulted in a “supercolonized” phenotype (Neubauer et al., 2017). Most of the differentiated TSR loci in our study were in ADAMTS‐like genes, a family of proteases involved in remodeling of the extracellular matrix (Kelwick, Desanlis, Wheeler, & Edwards, 2015).…”

“…Based on previous studies of symbiosis in Exaiptasia, we tested four gene sets for enrichment that had SNP markers in at least three genes in our dataset. These gene sets included a list of scavenger receptors (three genes present; Neubauer, Poole, Weis, & Davy, 2016), genes involved in the complement pathway (three genes present; Baumgarten et al, 2015), genes encoding proteins with thrombospondin-type-1 repeat motifs (14 genes present; Neubauer et al, 2017), and genes differentially regulated in larvae during symbiosis establishment (38 genes present;Wolfowicz et al, 2016).…”

Polymorphic adaptations in metazoans to establish and maintain photosymbioses

“…In corals, detailed work unravelling the genomic adaptations that enable photosymbiosis has increased our understanding of the onset and maintenance of this symbiosis significantly (Baumgarten et al, 2015;Neubauer et al, 2016Neubauer et al, , 2017van der Burg et al, 2016). Discrimination by the coral host among symbionts, pathogens, and food particles is key to symbiosis establishment and depends most likely on features of the host innate immune system (Davy, Allemand & Weis, 2012).…”

“…Photograph credits: Heike Wägele (Didemnum, Costasiella, Phyllodesmium, Tridacna, Briareum, Haliclona), João Serôdio (Symsagittifera) and Jenny Melo (Ambystoma). that is absent in non-symbiotic species: a repertoire of thrombospondin-type-1 repeat protein (TSR) (Neubauer et al, 2017) and a set of expanded scavenger receptors (SRs), including a unique c-type lectin domain (LOX1), several scavenger receptor cystein-rich (SRCR) receptors, and a specific set of Class B scavenger receptors (CD36) (Neubauer et al, 2016). Experimental studies on SRs and TSRs support their role in symbiont recognition (Rodriguez-Lanetty, Phillips & Weis, 2006;Lehnert et al, 2014;Neubauer et al, 2016Neubauer et al, , 2017.…”