Borrowed real estate: Sappinia lukoli, a new species of dung-dwelling amoeba that aggregates and hijacks the fruiting bodies of phylogenetically distant sorocarpic protists

Abstract

Upon defecation, dung enters the world as a short-lived bounty of nutrients. Yet, it becomes increasingly hostile as it ages. In two days dung can be dominated by predatory insect larvae, mites, nematodes, zoopagalean fungi, and toxin-producing bacteria. With rapidly changing chemical composition and dehydration, this environment becomes inhospitable to the life it originally hosted. It is in these contexts that we see a remarkable pattern in dung's protist diversity: across at least four eukaryotic supergroups, dung-dwelling amoeboid species have independently evolved cooperative behaviors by which cells navigate to the surface and form multicellular aggregates. Here we present a nuanced case of this behavioral diversity by describing Sappinia lukoli, a new amoeba species within Amoebozoa isolated from cattle dung. Other Sappinia species tend to be large and able to 'stand' by pushing their cell bodies into the open air. S. lukoli is the smallest Sappinia species described to date and does not stand. Instead, its cells aggregate at the distal tips of dung fibers and remain there as the culture ages. We also find that S. lukoli eats other dung-dwelling protists such as Sorodiplophrys stercorea (supergroup Stramenopiles) and Guttulinopsis vulgaris (supergroup Rhizaria). Strikingly, S. lukoli will gather inside the multicellular fruiting bodies built by S. stercorea and G. vulgaris on the dung surface. The cells of S. lukoli pack between host spores, effectively hijacking their fruiting bodies and gaining access to dispersal vectors. To our knowledge, this is the first record of a protist colonizing the aggregative fruiting bodies of other protists across multiple eukaryotic supergroups. S. lukoli's own aggregation is yet another independent origin of this behavior in dung, and we propose that the habitat itself repeatedly selects for cooperation among its microbial residents.