Evolution of Multicellular Complexity in The Dictyostelid Social Amoebas

Overview

Journal Genes (Basel)

Publisher MDPI

Date 2021 Apr 3

PMID 33801615

Citations 12

Authors

Koryu Kin

Pauline Schaap

Affiliations

Soon will be listed here.

Abstract

Multicellularity evolved repeatedly in the history of life, but how it unfolded varies greatly between different lineages. Dictyostelid social amoebas offer a good system to study the evolution of multicellular complexity, with a well-resolved phylogeny and molecular genetic tools being available. We compare the life cycles of the Dictyostelids with closely related amoebozoans to show that complex life cycles were already present in the unicellular common ancestor of Dictyostelids. We propose frost resistance as an early driver of multicellular evolution in Dictyostelids and show that the cell signalling pathways for differentiating spore and stalk cells evolved from that for encystation. The stalk cell differentiation program was further modified, possibly through gene duplication, to evolve a new cell type, cup cells, in Group 4 Dictyostelids. Studies in various multicellular organisms, including Dictyostelids, volvocine algae, and metazoans, suggest as a common principle in the evolution of multicellular complexity that unicellular regulatory programs for adapting to environmental change serve as "proto-cell types" for subsequent evolution of multicellular organisms. Later, new cell types could further evolve by duplicating and diversifying the "proto-cell type" gene regulatory networks.

Citing Articles

Limitations of 18S rDNA Sequence in Species-Level Classification of Dictyostelids.

Chittavichai T, Sathitnaitham S, Utthiya S, Prompichai W, Prommarit K, Vuttipongchaikij S Microorganisms. 2025; 13(2).

PMID: 40005642 PMC: 11857562. DOI: 10.3390/microorganisms13020275.

Amoebae: beyond pathogens- exploring their benefits and future potential.

Dinda S, Hazra S, De A, Datta A, Das L, Pattanayak S Front Cell Infect Microbiol. 2025; 14():1518925.

PMID: 39744153 PMC: 11688213. DOI: 10.3389/fcimb.2024.1518925.

Molecular Characterization of Ancient Prosaposin-like Proteins from the Protist .

Ortjohann M, Leippe M Biochemistry. 2024; 63(21):2768-2777.

PMID: 39421968 PMC: 11542183. DOI: 10.1021/acs.biochem.4c00479.

Life cycle strategies in free-living unicellular eukaryotes: Diversity, evolution, and current molecular tools to unravel the private life of microorganisms.

Rizos I, Frada M, Bittner L, Not F J Eukaryot Microbiol. 2024; 71(6):e13052.

PMID: 39085163 PMC: 11603280. DOI: 10.1111/jeu.13052.

Ion Signaling in Cell Motility and Development in .

Morimoto Y Biomolecules. 2024; 14(7).

PMID: 39062545 PMC: 11274586. DOI: 10.3390/biom14070830.

References

Schaap P . Quantitative analysis of the spatial distribution of ultrastructural differentiation markers during development ofDictyostelium discoideum. Wilehm Roux Arch Dev Biol. 2017; 192(2):86-94. DOI: 10.1007/BF00848484. View

Stanley S . An ecological theory for the sudden origin of multicellular life in the late precambrian. Proc Natl Acad Sci U S A. 1973; 70(5):1486-9. PMC: 433525. DOI: 10.1073/pnas.70.5.1486. View

Du Q, Schilde C, Birgersson E, Chen Z, McElroy S, Schaap P . The cyclic AMP phosphodiesterase RegA critically regulates encystation in social and pathogenic amoebas. Cell Signal. 2013; 26(2):453-9. PMC: 3906536. DOI: 10.1016/j.cellsig.2013.10.008. View

Nedelcu A, Michod R . Stress Responses Co-Opted for Specialized Cell Types During the Early Evolution of Multicellularity: The Role of Stress in the Evolution of Cell Types Can Be Traced Back to the Early Evolution of Multicellularity. Bioessays. 2020; 42(5):e2000029. DOI: 10.1002/bies.202000029. View

Sebe-Pedros A, Degnan B, Ruiz-Trillo I . The origin of Metazoa: a unicellular perspective. Nat Rev Genet. 2017; 18(8):498-512. DOI: 10.1038/nrg.2017.21. View

Schaap P, Schilde C . Encystation: the most prevalent and underinvestigated differentiation pathway of eukaryotes. Microbiology (Reading). 2018; 164(5):727-739. DOI: 10.1099/mic.0.000653. View

El Albani A, Bengtson S, Canfield D, Bekker A, Macchiarelli R, Mazurier A . Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago. Nature. 2010; 466(7302):100-4. DOI: 10.1038/nature09166. View

Konig S, Nedelcu A . The genetic basis for the evolution of soma: mechanistic evidence for the co-option of a stress-induced gene into a developmental master regulator. Proc Biol Sci. 2020; 287(1940):20201414. PMC: 7739920. DOI: 10.1098/rspb.2020.1414. View

Pitt G, Milona N, Borleis J, Lin K, Reed R, Devreotes P . Structurally distinct and stage-specific adenylyl cyclase genes play different roles in Dictyostelium development. Cell. 1992; 69(2):305-15. DOI: 10.1016/0092-8674(92)90411-5. View

10.

Ratcliff W, Ford Denison R, Borrello M, Travisano M . Experimental evolution of multicellularity. Proc Natl Acad Sci U S A. 2012; 109(5):1595-600. PMC: 3277146. DOI: 10.1073/pnas.1115323109. View

11.

Ostrowski E . Enforcing Cooperation in the Social Amoebae. Curr Biol. 2019; 29(11):R474-R484. DOI: 10.1016/j.cub.2019.04.022. View

12.

Medina J, Shreenidhi P, Larsen T, Queller D, Strassmann J . Cooperation and conflict in the social amoeba Dictyostelium discoideum. Int J Dev Biol. 2019; 63(8-9-10):371-382. DOI: 10.1387/ijdb.190158jm. View

13.

Claessen D, Rozen D, Kuipers O, Sogaard-Andersen L, van Wezel G . Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nat Rev Microbiol. 2014; 12(2):115-24. DOI: 10.1038/nrmicro3178. View

14.

Fritz-Laylin L, Prochnik S, Ginger M, Dacks J, Carpenter M, Field M . The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell. 2010; 140(5):631-42. DOI: 10.1016/j.cell.2010.01.032. View

15.

Herron M, Borin J, Boswell J, Walker J, Chen I, Knox C . De novo origins of multicellularity in response to predation. Sci Rep. 2019; 9(1):2328. PMC: 6382799. DOI: 10.1038/s41598-019-39558-8. View

16.

Schlichting C . Origins of differentiation via phenotypic plasticity. Evol Dev. 2002; 5(1):98-105. DOI: 10.1046/j.1525-142x.2003.03015.x. View

17.

Benabentos R, Hirose S, Sucgang R, Curk T, Katoh M, Ostrowski E . Polymorphic members of the lag gene family mediate kin discrimination in Dictyostelium. Curr Biol. 2009; 19(7):567-72. PMC: 2694408. DOI: 10.1016/j.cub.2009.02.037. View

18.

El Albani A, Mangano M, Buatois L, Bengtson S, Riboulleau A, Bekker A . Organism motility in an oxygenated shallow-marine environment 2.1 billion years ago. Proc Natl Acad Sci U S A. 2019; 116(9):3431-3436. PMC: 6397584. DOI: 10.1073/pnas.1815721116. View

19.

Chavez L, BALAMUTH W, Gong T . A light and electron microscopical study of a new, polymorphic free-living amoeba, Phreatamoeba balamuthi n. g., n. sp. J Protozool. 1986; 33(3):397-404. DOI: 10.1111/j.1550-7408.1986.tb05630.x. View

20.

Bloomfield G, Skelton J, Ivens A, Tanaka Y, Kay R . Sex determination in the social amoeba Dictyostelium discoideum. Science. 2010; 330(6010):1533-6. PMC: 3648785. DOI: 10.1126/science.1197423. View