Insights into the origin of metazoan multicellularity from predatory unicellular relatives of animals

Abstract

Background: The origin of animals from their unicellular ancestor was one of the most important events in evolutionary history, but the nature and the order of events leading up to the emergence of multicellular animals are still highly uncertain. The diversity and biology of unicellular relatives of animals have strongly informed our understanding of the transition from single-celled organisms to the multicellular Metazoa. Here, we analyze the cellular structures and complex life cycles of the novel unicellular holozoans Pigoraptor and Syssomonas (Opisthokonta), and their implications for the origin of animals. Results: Syssomonas and Pigoraptor are characterized by complex life cycles with a variety of cell types including flagellates, amoeboflagellates, amoeboid non-flagellar cells, and spherical cysts. The life cycles also include the formation of multicellular aggregations and syncytium-like structures, and an unusual diet for single-celled opisthokonts (partial cell fusion and joint sucking of a large eukaryotic prey), all of which provide new insights into the origin of multicellularity in Metazoa. Several existing models explaining the origin of multicellular animals have been put forward, but these data are interestingly consistent with one, the "synzoospore hypothesis." Conclusions: The feeding modes of the ancestral metazoan may have been more complex than previously thought, including not only bacterial prey, but also larger eukaryotic cells and organic structures. The ability to feed on large eukaryotic prey could have been a powerful trigger in the formation and development of both aggregative (e.g., joint feeding, which also implies signaling) and clonal (e.g., hypertrophic growth followed by palintomy) multicellular stages that played important roles in the emergence of multicellular animals.

Interplay of mesoscale physics and agent-like behaviors in the parallel evolution of aggregative multicellularity

“…Our broader concept of homology can potentially help resolve enigmas of biological similarity across phylogenetic distances. While some of the closest relatives of the metazoans, extant holozoans, exhibit clonal multicellularity [ 188 , 189 ], others exhibit behaviors consistent with the idea that the animals may have arisen from unicellular ancestors by aggregation [ 188 – 190 ]. Knowledge of molecular and cellular determinants of material identity and agent-like behaviors in aggregative microorganisms, in concert with suitable mathematical and computational models of these causally hybrid, multiscale systems (e.g., [ 98 , 191 ]), could help forge a testable and potentially universal account of morphological evolution.…”

A flagellate-to-amoeboid switch in the closest living relatives of animals

“…Salpingoeca helianthica generated very large and branched blebs (Fig. 4a,b; Supplementary Video 16), often longer than the rest of the cell body – reminiscent of the “lobopods” described in some protists 38 . Finally, Salpingoeca urceolata (Fig.…”

“…in phagocytes patrolling tissues 14 ). Cell crawling has also been frequently observed in the sister-lineage of choanozoans, filastereans 36–38 – but its seeming absence from choanoflagellates had made its evolutionary history unclear. Together with the existing comparative evidence, our data suggest that the last common ancestor of choanoflagellates and animals had the ability to differentiate into amoeboid and amoeboflagellate cells under confinement.…”

“…Consistent with an ancient origin of all three phenotypes, amoeboid, flagellate and amoeboflagellate cells are all broadly distributed in opisthokonts (animals, fungi, and their relatives). Interestingly, amoeboflagellate phenotypes have recently been described in several species occupying key phylogenetic positions, including in the sister-group of choanozoans (the filastereans) 37,38 , in early-branching fungi 39,68,69 , in the two closest known relatives of opisthokonts (apusomonads 70 and breviates 71 ), and in early-branching amoebozoans 72 . This is consistent with an ancient origin and broad conservation of the amoeboflagellate phenotype in opisthokonts 73 .…”

“…This is consistent with an ancient origin and broad conservation of the amoeboflagellate phenotype in opisthokonts 73 . Opisthokont ancestors might have crawled using a combination of blebs (as in amoeboid choanoflagellates, amoeboid animal cells 9,11 , and amoebozoans 44 ), pseudopods (which are present in choanoflagellates during phagocytosis 22,39 and during crawling in chytrid fungi 8,39 , amoebozoans 44 , and some holozoans 38 ), and filopodia (which contribute to locomotion in filastereans 63 and choanoflagellate settlement 30 ). Moreover, cell crawling is regulated by confinement in animal cells 9–12 , choanoflagellates, chytrid fungi 39 and dictyostelid amoebozoans 44 , suggesting that the ability to respond to confinement might be an ancient feature.…”