Cell Biology: Molecular clue links bacteria to the origin of animals
Over the last decade, phylogeneticists have reached a consensus about the branch of the tree of life that includes the fungi, the choanoflagellates and the animals (Parfrey et al., 2010). It is now clear that the choanoflagellates—aquatic organisms that contain just one or a few cells—and the animals are sister groups, which strongly suggests that animal multicellularity evolved within ancient choanoflagellates (Carr et al., 2008). Research by Nicole King of the University of California at Berkeley has shown that a single-celled species of choanoflagellate, Salpingoeca rosetta, can also exist in organized colonies, which are called rosettes (see Figure 1; King, 2004). Exploring the factors that cause the transition from single cells to colonies, King and co-workers have identified bacterial strains that serve as food for the choanoflagellates and induce the formation of colonies (Fairclough et al., 2010), and recently they described a new species of bacteria that is capable of inducing colony formation (Alegado et al., 2012b). Now, as reported in eLife, a collaboration led by King and Jon Clardy of Harvard Medical School has determined the identities of multiple bacterial species from a single phylum (the Bacteroidetes) that can induce these transitions. They have also established the chemical nature of molecules produced by the bacteria that are responsible for inducing colony formation in S. rosetta (Alegado et al., 2012a).

Electron micrographs showing single choanoflagellates (left; scale bar is 2 microns) and a colony of choanoflagellates (right; scale bar is 5 microns). The release of a sulfonolipid molecule by Algoriphagus bacteria that live among the choanoflagellates is thought to trigger the formation of the colonies.
FIGURE CREDIT: ROSIE ALEGADO (LEFT); MARK DAYEL (RIGHT).
While multicellularity must have arisen numerous times during evolution, this latest advance is notable because it exposes the role of bacteria in the process. Perhaps we should not be surprised, because bacteria had the earth to themselves for at least a billion years before single-celled eukaryotes evolved from and among them, and it is likely that bacteria were involved in all aspects of the lives of the early protists, including the beginnings of colony formation. However, it is surprising that bacteria have a role as central as that revealed in this work.
What is especially interesting about the bacteria-induced formation of colonies in S. rosetta is that it happens as a result of incomplete cell division, starting with a single cell, rather than the aggregation individual cells (Fairclough et al., 2010; Dayel et al. 2011). The process is thus reminiscent of animal embryology. Moreover, the cells in these choanoflagellate colonies reside within a common extracelluar matrix and are connected to each other by short (∼1 µm), complex intercellular bridges, much like those found between cells in many animal tissues (Dayel et al., 2011).
The collaboration, which includes Rosie Alegado of Berkeley and Laura Brown of Harvard as joint first authors, describes the complex process through which they isolated and identified the bacterial molecule that induces the transformation (Alegado et al., 2012a). The molecule is a sulfonolipid with the chemical formula C32H64NO7S. They speculate that this bacterial sulfonolipid has a highly specific receptor on the choanoflagellate surface, and that the binding of the sulfonolipid molecule to this receptor, which peaks at concentrations in the femtomolar range, may be related to feeding advantages enjoyed by the rosette-colony phase. The discovery of this distinct role for a sulfonolipid is certain to spur research on the occurrence and function of these compounds in many groups of organisms.
A major role for bacteria in colony formation in the closest living relatives of animals suggests another avenue of research, namely on the development of sponges. A major cell type in all sponges, the choanocyte, bears remarkable structural and functional similarity with the choanoflagellates, and this suggests a close evolutionary history between the two. The sponges, which are recognized as the simplest and probably most ancient of the animals, are hosts to many bacterial species: indeed, bacteria can make up more than 40% of the volume of an individual. Moreover, many bacterial species are transmitted, via embryos and larvae, from one generation of sponges to the next. There is also an intimate and complex relationship between cyanobacteria (bacteria that obtain their energy from photosynthesis) and the embryos of their sponge host. Furthermore, bacterial cells have also been observed in the intracellular vacuoles of developing sponges (see Thacker and Freeman, 2012 for a review of research into the interactions between sponges and microbes). All this work suggests a number of questions: do the interactions between bacteria and developing embryos in sponges have a role that is similar to the role played by bacteria in the formation of multicellular colonies in S. rosetta? Are symbiotic bacteria essential for normal sponge development?
The new insights into the interactions between bacteria and the earliest ancestors of the animals revealed by Alegado and co-authors, along with our growing understanding of the relationships between bacteria and sponges, should remind all biologists that bacteria are responsible for more than their impacts on our health—without them, our single-celled ancestors might never have made the transition to multicellularity. Like those early choanoflagellates, all living animals exist in a world filled with bacteria, and these bacteria are likely to be having an impact on many aspects of their biology.
References
-
A bacterial sulfonolipid triggers multicellular development in the closest living relatives of animalseLife 1:e00013.
-
Algoriphagus machipongonensis sp. nov. co-isolated with a colonial choanoflagellateInt J Syst Evol Microbiol.
-
Molecular phylogeny of choanoflagellates, the sister group to MetazoaProc Natl Acad Sci USA 105:16641–16646.
-
Cell differentiation and morphogenesis in the colony-forming choanoflagellateSalpingoeca rosetta. Dev Biol 357:73–82.
-
Broadly sampled multigene analyses yield a well-resolved eukaryotic tree of lifeSyst Biol 59:518–533.
Article and author information
Author details
Publication history
- Version of Record published: October 15, 2012 (version 1)
Copyright
© 2012, Hadfield
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 593
- Page views
-
- 96
- Downloads
-
- 0
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
Bacteria might have influenced the origin of multicellularity in animals.
-
- Cell Biology
Uso1/p115 and RAB1 tether ER-derived vesicles to the Golgi. Uso1/p115 contains a globular-head-domain (GHD), a coiled-coil (CC) mediating dimerization/tethering and a C-terminal region (CTR) interacting with golgins. Uso1/p115 is recruited to vesicles by RAB1. Genetic studies placed Uso1 paradoxically acting upstream of, or in conjunction with RAB1 (Sapperstein et al., 1996). We selected two missense mutations in uso1 resulting in E6K and G540S in the GHD that rescued lethality of rab1-deficient Aspergillus nidulans. The mutations are phenotypically additive, their combination suppressing the complete absence of RAB1, which emphasizes the key physiological role of the GHD. In living hyphae Uso1 recurs on puncta (60 sec half-life) colocalizing partially with the Golgi markers RAB1, Sed5 and GeaA/Gea1/Gea2, and totally with the retrograde cargo receptor Rer1, consistent with Uso1 dwelling in a very early Golgi compartment from which ER residents reaching the Golgi recycled back to the ER. Localization of Uso1, but not of Uso1E6K/G540S, to puncta is abolished by compromising RAB1 function, indicating that E6K/G540S creates interactions bypassing RAB1. That Uso1 delocalization correlates with a decrease in the number of Gea1 cisternae supports that Uso1-and-Rer1-containing puncta are where the protein exerts its physiological role. In S-tag-coprecipitation experiments Uso1 is an associate of the Sed5/Bos1/Bet1/Sec22 SNARE complex zippering vesicles with the Golgi, with Uso1E6K/G540S showing stronger association. Using purified proteins, we show that Bos1 and Bet1 bind the Uso1 GHD directly. However, Bet1 is a strong E6K/G540S-independent binder, whereas Bos1 is weaker but becomes as strong as Bet1 when the GHD carries E6K/G540S. G540S alone markedly increases GHD binding to Bos1, whereas E6K causes a weaker effect, correlating with their phenotypic contributions. AlphaFold2 predicts that G540S increases binding of the GHD to the Bos1 Habc domain. In contrast, E6K lies in an N-terminal, potentially alpha-helical, region that sensitive genetic tests indicate as required for full Uso1 function. Remarkably, this region is at the end of the GHD basket opposite to the end predicted to interact with Bos1. We show that unlike dimeric full-length and CTR∆ Uso1 proteins, the GHD lacking the CC/CTR dimerization domain, whether originating from bacteria or Aspergillus extracts and irrespective of whether it carries or not E6K/G540S, would appear to be monomeric. With the finding that overexpression of E6K/G540S and wild-type GHD complement uso1∆, our data indicate that the GHD monomer is capable of providing, at least partially, the essential Uso1 functions, and that long-range tethering activity is dispensable. Rather, these findings strongly suggest that the essential role of Uso1 involves the regulation of SNAREs.