The emergence of multicellular organisms has been one of the major transitions during the evolutionary history of life on Earth (Smith and Szathmáry, 1995), with multicellularity evolving several times independently in the Tree of Life (Grosberg and Strathmann, 2007; Bonner, 2009; Niklas and Newman, 2013). Multicellularity can be simply defined as the result of cellular aggregation (Schirrmeister et al., 2013) or, if more stringent criteria are taken into account, as a coordinated behavior involving cell-to-cell interconnection, communication, cooperation, and differentiation (Kaiser, 2001; Wolpert and Szathmáry, 2002). For this reason, both complex organisms such as fungi, plants and animals, and, to some extent, simple microbial systems like colonial protists and biofilm-forming bacteria are considered multicellular (Grosberg and Strathmann, 2007; Hengge, 2020). Unveiling the circumstances that caused unicellular organisms to evolve complex multicellularity and the molecular mechanisms that supported this transition is extremely challenging, considering that the first steps occurred more than 200 million years ago for plants, and 600 million years ago for animals (Herron et al., 2009; Ros-Rocher et al., 2021). Although researchers from various disciplines have studied this question for several decades, many unanswered questions remain about why unicellular organisms formed multicellular beings so frequently during evolution, which regulatory changes supported this profound change, and how organisms overcame individual self-interest in favor of altruistic or synergistic cooperation. Typically, two changes are considered essential for the evolution of complex multicellularity: cell-cell adhesion and intercellular communication leading to coordinated action. These traits are common in unicellular species with a facultative multicellular life stage, such as green algae, fungi, slime molds, and choanoflagellates [reviewed in Brunet and King (2017)]. Indeed, many of these species show differentiation across their life cycle that, at some level, may be interpreted as developmental, although they do not involve communication among cells as sophisticated as that of multicellular organisms or cell death. Even obligate unicellular organisms can display traits that are linked to the emergence of multicellularity, such as intercellular communication, cell-cell adhesion, and differentiation into distinct developmental stages during their (a)sexual life cycles. These characteristics have been exploited in some unicellular groups, such as the yeast Saccharomyces cerevisiae, to explore the early phases of multicellularity through experimental evolution (Ratcliff et al., 2012). Through this Research Topic, “Unicellular Organisms As An Evolutionary Snapshot Toward Multicellularity,” which consists of three Original Research articles and two Hypothesis and Theory articles (Figure 1), we wanted to emphasize the study of unicellular and simple multicellular organisms as an additional approach to understand the molecular mechanisms at the basis of multicellularity.

Editorial: Unicellular organisms as an evolutionary snapshot toward multicellularity

Marotta P.
;
2023

Abstract

The emergence of multicellular organisms has been one of the major transitions during the evolutionary history of life on Earth (Smith and Szathmáry, 1995), with multicellularity evolving several times independently in the Tree of Life (Grosberg and Strathmann, 2007; Bonner, 2009; Niklas and Newman, 2013). Multicellularity can be simply defined as the result of cellular aggregation (Schirrmeister et al., 2013) or, if more stringent criteria are taken into account, as a coordinated behavior involving cell-to-cell interconnection, communication, cooperation, and differentiation (Kaiser, 2001; Wolpert and Szathmáry, 2002). For this reason, both complex organisms such as fungi, plants and animals, and, to some extent, simple microbial systems like colonial protists and biofilm-forming bacteria are considered multicellular (Grosberg and Strathmann, 2007; Hengge, 2020). Unveiling the circumstances that caused unicellular organisms to evolve complex multicellularity and the molecular mechanisms that supported this transition is extremely challenging, considering that the first steps occurred more than 200 million years ago for plants, and 600 million years ago for animals (Herron et al., 2009; Ros-Rocher et al., 2021). Although researchers from various disciplines have studied this question for several decades, many unanswered questions remain about why unicellular organisms formed multicellular beings so frequently during evolution, which regulatory changes supported this profound change, and how organisms overcame individual self-interest in favor of altruistic or synergistic cooperation. Typically, two changes are considered essential for the evolution of complex multicellularity: cell-cell adhesion and intercellular communication leading to coordinated action. These traits are common in unicellular species with a facultative multicellular life stage, such as green algae, fungi, slime molds, and choanoflagellates [reviewed in Brunet and King (2017)]. Indeed, many of these species show differentiation across their life cycle that, at some level, may be interpreted as developmental, although they do not involve communication among cells as sophisticated as that of multicellular organisms or cell death. Even obligate unicellular organisms can display traits that are linked to the emergence of multicellularity, such as intercellular communication, cell-cell adhesion, and differentiation into distinct developmental stages during their (a)sexual life cycles. These characteristics have been exploited in some unicellular groups, such as the yeast Saccharomyces cerevisiae, to explore the early phases of multicellularity through experimental evolution (Ratcliff et al., 2012). Through this Research Topic, “Unicellular Organisms As An Evolutionary Snapshot Toward Multicellularity,” which consists of three Original Research articles and two Hypothesis and Theory articles (Figure 1), we wanted to emphasize the study of unicellular and simple multicellular organisms as an additional approach to understand the molecular mechanisms at the basis of multicellularity.
2023
Istituto di Biochimica e Biologia Cellulare - IBBC
cell cooperation
development
differentiation
evolution
multicellular organism
unicellular organism
File in questo prodotto:
File Dimensione Formato  
fcell-11-1254636.pdf

accesso aperto

Tipologia: Versione Editoriale (PDF)
Licenza: Creative commons
Dimensione 888.82 kB
Formato Adobe PDF
888.82 kB Adobe PDF Visualizza/Apri

I documenti in IRIS sono protetti da copyright e tutti i diritti sono riservati, salvo diversa indicazione.

Utilizza questo identificativo per citare o creare un link a questo documento: https://hdl.handle.net/20.500.14243/516921
Citazioni
  • ???jsp.display-item.citation.pmc??? ND
  • Scopus 0
  • ???jsp.display-item.citation.isi??? ND
social impact