The origin of animals: an ancestral reconstruction of the unicellular-to-multicellular transition

Ros-Rocher, Núria; Pérez-Posada, Alberto; Leger, Michelle M.; Ruiz‐Trillo, Iñaki

doi:10.1098/rsob.200359

Cited by 79 publications

(64 citation statements)

References 243 publications

(652 reference statements)

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“…Multiple approaches have been used to characterize functions, morphology, and diversity of cell types in representatives of each metazoan phylum as well as in unicellular holozoans in order to gain insight into the evolutionary origins of Metazoa (reviewed by 53 , 106 – 112 ). Four somatic cell types previously have been identified in representatives of all animal phyla: squamous/cuboidal/columnar epithelial cells that form a protective barrier, absorptive epithelial cells that take up nutrients, mucocytes that secrete mucus, and sensory cells that secrete peptides and/or small molecular transmitters 14 , 20 , 24 , 62 , 76 , 113 – 122 .…”

Section: Discussionmentioning

confidence: 99%

Placozoan fiber cells: mediators of innate immunity and participants in wound healing

Mayorova

Hammar

Jung

et al. 2021

Sci Rep

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Placozoa is a phylum of non-bilaterian marine animals. These small, flat organisms adhere to the substrate via their densely ciliated ventral epithelium, which mediates mucociliary locomotion and nutrient uptake. They have only six morphological cell types, including one, fiber cells, for which functional data is lacking. Fiber cells are non-epithelial cells with multiple processes. We used electron and light microscopic approaches to unravel the roles of fiber cells in Trichoplax adhaerens, a representative member of the phylum. Three-dimensional reconstructions of serial sections of Trichoplax showed that each fiber cell is in contact with several other cells. Examination of fiber cells in thin sections and observations of live dissociated fiber cells demonstrated that they phagocytose cell debris and bacteria. In situ hybridization confirmed that fiber cells express genes involved in phagocytic activity. Fiber cells also are involved in wound healing as evidenced from microsurgery experiments. Based on these observations we conclude that fiber cells are multi-purpose macrophage-like cells. Macrophage-like cells have been described in Porifera, Ctenophora, and Cnidaria and are widespread among Bilateria, but our study is the first to show that Placozoa possesses this cell type. The phylogenetic distribution of macrophage-like cells suggests that they appeared early in metazoan evolution.

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Section: Discussionmentioning

confidence: 99%

Placozoan fiber cells: mediators of innate immunity and participants in wound healing

Mayorova

Hammar

Jung

et al. 2021

Sci Rep

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“…We did not detect CMAH in any choanoflagellates (the sister group to animals) or other nonanimal holozoan species but only in protists even less closely related to animals (Figure 2). If we assume sponges are the earliest known branch of animals [27], CMAH might have been one of the genetic novelties present in the lineage that led to animals, present in the last common ancestor of animals but not in the (earlier) last unicellular ancestor of animals [28]. We posit that Neu5Gc presence might have shaped the relationships between animals and their pathogens since the Metazoa kingdom evolved.…”

Section: Neu5gc Vs Neu5acmentioning

confidence: 95%

Sialic Acids as Receptors for Pathogens

et al. 2021

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Carbohydrates have long been known to mediate intracellular interactions, whether within one organism or between different organisms. Sialic acids (Sias) are carbohydrates that usually occupy the terminal positions in longer carbohydrate chains, which makes them common recognition targets mediating these interactions. In this review, we summarize the knowledge about animal disease-causing agents such as viruses, bacteria and protozoa (including the malaria parasite Plasmodium falciparum) in which Sias play a role in infection biology. While Sias may promote binding of, e.g., influenza viruses and SV40, they act as decoys for betacoronaviruses. The presence of two common forms of Sias, Neu5Ac and Neu5Gc, is species-specific, and in humans, the enzyme converting Neu5Ac to Neu5Gc (CMAH, CMP-Neu5Ac hydroxylase) is lost, most likely due to adaptation to pathogen regimes; we discuss the research about the influence of malaria on this trait. In addition, we present data suggesting the CMAH gene was probably present in the ancestor of animals, shedding light on its glycobiology. We predict that a better understanding of the role of Sias in disease vectors would lead to more effective clinical interventions.

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“…In all cases, the transition from the unicellular to a multicellular stage is a response to environmental cues. Moreover, even stages of highly sophisticated and integrated developmental animal life cycles have been discovered to depend on external factors and ecological triggers, some of which are based on communication with external bacteria (25). Theoretical models of life cycle evolution have shown that a changing environment can lead to the evolution of complex life cycles in which some cells live and reproduce as unicellular beings, while others form groups (26).…”

Section: Phenotypic Plasticity and Evolutionary Transitions In Multicellularitymentioning

confidence: 99%

Phenotypic plasticity, life cycles, and the evolutionary transition to multicellularity

S¹,

Pichugin

Hammerschmidt³

2021

Preprint

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Understanding the evolutionary transition to multicellularity is a key problem in evolutionary biology (1,2). While around 25 independent instances of the evolution of multicellular existence are known across the tree of life (3), the ecological conditions that drive such transformations are not well understood. The first known transition to multicellularity occurred approximately 2.5 billion years ago in cyanobacteria (4,5,6), and today's cyanobacteria are characterized by an enormous morphological diversity, ranging from single-celled species over simple filamentous to highly differentiated filamentous ones (7,8). While the cyanobacterium Cyanothece sp. ATCC 51142 was isolated from the intertidal zone of the U.S. Gulf Coast as a unicellular species (9), we are first to additionally report a phenotypically mixed strategy where multicellular filaments and unicellular stages alternate. We experimentally demonstrate that the facultative multicellular life cycle depends on environmental conditions, such as salinity and population density, and use a theoretical model to explore the process of filament dissolution. While results predict that the observed response can be caused by an excreted compound in the medium, we cannot fully exclude changes in nutrient availability (as in (10,11)). The best fit modeling results demonstrate a nonlinear effect of the compound, which is characteristic for density-dependent sensing systems (12,13). Further, filament fragmentation is predicted to occur by means of connection cleavage rather than by cell death of every alternate cell. The phenotypic switch between the single-celled and multicellular morphology constitutes an environmentally dependent life cycle, which likely represents an important step en route to permanent multicellularity.

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The origin of animals: an ancestral reconstruction of the unicellular-to-multicellular transition

Cited by 79 publications

References 243 publications

Placozoan fiber cells: mediators of innate immunity and participants in wound healing

Placozoan fiber cells: mediators of innate immunity and participants in wound healing

Sialic Acids as Receptors for Pathogens

Phenotypic plasticity, life cycles, and the evolutionary transition to multicellularity

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