Bacterial influences on animal origins

Abstract

Animals evolved in seas teeming with bacteria, yet the influences of bacteria on animal origins are poorly understood. Comparisons among modern animals and their closest living relatives, the choanoflagellates, suggest that the first animals used flagellated collar cells to capture bacterial prey. The cell biology of prey capture, such as cell adhesion between predator and prey, involves mechanisms that may have been co-opted to mediate intercellular interactions during the evolution of animal multicellularity. Moreover, a history of bacterivory may have influenced the evolution of animal genomes by driving the evolution of genetic pathways for immunity and facilitating lateral gene transfer. Understanding the interactions between bacteria and the progenitors of animals may help to explain the myriad ways in which bacteria shape the biology of modern animals, including ourselves.

Figure 1.

Major events in life’s history influenced by bacteria. Bacteria have exerted critical influences on the evolution of eukaryotes and, ultimately, the origin and evolution of animals (processes indicated in gray bubbles). Bacteria and archaea contributed to the cellular and genetic building blocks for the first eukaryotic cells, and bacteria formed stable associations with early eukaryotes in the form of mitochondria and plastids. Moreover, bacteria were likely an important source of food for the progenitors of animals, as well as the first animals themselves. Finally, photosynthetic bacteria were critical for shaping the environment in which animals would evolve. The Great Oxygenation Event, estimated to have occurred 2.3 billion years ago, is likely to have been fueled by photosynthetic cyanobacteria. Moreover, photosynthetically derived oxygen, coupled with underlying geochemical processes, lead to episodic increases in oxygen levels starting in the Proterozoic. The timeline (rectangle) depicts the predominant redox state of the oceans. Anoxic surface and deep ocean waters (black) dominated the Archean Eon. During the Proterozoic Eon, surface waters became oxygenated because of mixing; however, the deep oceans remained anoxic (green). Isotopic measurements of sediments suggest that the chemistry of the ocean between ∼1.8 Gya and 1 Gya was sulfidic and ferruginous (red). This period also marked the height of stromatolite abundance and diversity before their decline in the Neoproterozoic period. The Neoproterozoic is marked by the appearance of Ediacaran biota and periods of glaciation. During the Phanerozoic, more widespread oxygenation of surface and deep waters (blue) was roughly concomitant with the emergence of animals around 635 million years ago. Phan., Phanerozoic.

Figure 2.

Ancestry and evolution of animal–bacterial interactions. Bacterial influences on the origin and evolution of animals can be inferred by comparing the organismal biology and genome content of extant choanoflagellates and diverse animals within a robust phylogenetic framework (upper left). Features shared among choanoflagellates and diverse animals were likely present in their last common ancestor (Choano/Animal LCA, blue square; bottom right). Likewise, the biology of the Urmetazoan (purple square), Ureumetazoan (green square), and Urbilaterian (black square) can be reconstructed from features that are shared among diverse animals, eumetazoans (i.e., tissue-grade animals), and bilaterians, respectively. The conservation of collar cells in choanoflagellates, sponges, and diverse eumetazoa suggests that the progenitors of choanoflagellates and animals likely used collar cells to capture bacteria. Epithelia, an animal cell type that may be derived from an ancestral collar cell, are found in diverse animals and were likely present in the Urmetazoan. Pattern recognition protein domains, including TIR/Ig domains and C-type lectins, are expressed by diverse animals and likely evolved in stem animals, if not earlier. Interactions with bacteria were mediated solely at the cellular level in the Choano/Animal LCA and the Urmetazoan, whereas eumetazoans have evolved specialized tissue and organ systems, including the gut cavity, to harbor bacteria and regulate interactions with bacteria. Question marks indicate uncertainty about the presence or absence of a character for a given ancestor.

Figure 3.

Variations on a collar cell theme in choanoflagellates and animals. Collar cells are typified by the presence of a single apical flagellum (indicated with an arrow) surrounded by a collar of actin-filled microvilli (indicated with a bracket). (A) Choanoflagellates are heterotrophic microeukaryotes that undulate their apical flagellum to generate water currents that draw bacteria against their actin-filled collar before phagocytosis (image of Salpingoeca rosetta courtesy of Mark Dayel. (B) Like choanoflagellates, sponge collar cells also have a single apical flagellum and collar of microvilli that they use to capture bacterial prey (image of choanocyte chamber from Oscarella carmela courtesy of Scott Nichols). (C,D) Collar cells have also been observed in cnidarians (adapted from data in Lyons 1973) and (E,F) echinoderms (adapted from data in Nerrevang and Wingstrand 1970). Original labels for C: go, Golgi body; gr, granules; l, lipid; m, mucus; mv, collar microvilli; nu, nucleus; p, plaque, r, ciliary rootlet; t, cylindrical thickening; tw, terminal web; v, vacuole. Original labels for D: mu, mucus coat; v, vacuole. Original labels for E: B, basal bodies; C, collar; DP, dense plasma; EB, external branch of microvillus; F, flagellum; G, Golgi apparatus; MC, medium-contrast clumps without membrane; M, mitochondria; PV, phagocytic vacuole; TB, terminal bar; SJ septate junction. Original labels for F: MU, mucus; PV, phagocytic vacuole.

Figure 4.

Choanoflagellate colony development as a model for animal origins. (A) The evolution of animals from their single-celled ancestors is hypothesized to have involved a transition through a simple, flagellated colonial form termed the Blastaea by Ernst Haeckel (1874). (B) S. rosetta produces rosette-shaped colonies that resemble Haeckel’s hypothesized Blastaea (Dayel et al. 2011). (C) S. rosetta undergoes transient differentiation into slow swimming cells (1), attached “thecate” cells (4), fast swimmer cells (5), rosette colonies (2), and chain colonies (3) (adapted from data in Dayel et al. 2011). Arrows indicate differentiation events that have been observed under laboratory conditions. (D) A prey bacterium, Algoriphagus machipongonensis, produces a bioactive sulfonolipid, rosette-inducing factor-1 (RIF-1), that is sufficient to stimulate rosette colony development in S. rosetta (Alegado et al. 2012). (E) RIF-1 is composed of a fatty acid chain (black), capnoid base (red), and sulfonic acid head group (gray circle).