An Evo‐Devo Perspective on Multicellular Development of Myxobacteria

Abstract

The transition to multicellularity, recognized as one the major transitions in evolution, has occurred independently several times. While multicellular development has been extensively studied in zygotic organisms including plant and animal groups, just a few aggregative multicellular organisms have been employed as model organisms for the study of multicellularity. Studying different evolutionary origins and modes of multicellularity enables comparative analyses that can help identifying lineage-specific aspects of multicellular evolution and generic factors and mechanisms involved in the transition to multicellularity. Among aggregative multicellular organisms, myxobacteria are a valuable system to explore the particularities that aggregation confers to the evolution of multicellularity and mechanisms shared with clonal organisms. Moreover, myxobacteria species develop fruiting bodies displaying a range of morphological diversity. In this review, we aim to synthesize diverse lines of evidence regarding myxobacteria development and discuss them in the context of Evo-Devo concepts and approaches. First, we briefly describe the developmental processes in myxobacteria, present an updated comparative analysis of the genes involved in their developmental processes and discuss these and other lines of evidence in terms of co-option and developmental system drift, two concepts key to Evo-Devo studies. Next, as has been suggested from Evo-Devo approaches, we discuss how broad comparative studies and integration of diverse genetic, physicochemical, and environmental factors into experimental and theoretical models can further our understanding of myxobacterial development, phenotypic variation, and evolution.

Laboratory biases hinder Eco‐Evo‐Devo integration: Hints from the microbial world

“…Furthermore, in light of their ubiquity across environments and their diverse uni‐ and multicellular lifestyles, microorganisms can provide invaluable insights to further understanding organism–environment interactions and the processes generating the variation that enables evolution. Moreover, multicellular microbial groups can yield information about the organism–environment interactions during the evolution of multicellularity since they develop in a scale and environment similar to those in which multicellularity presumably emerged (Arias Del Angel, Escalante, Martínez‐Castilla, & Benítez, ; Bonner, ; Rivera‐Yoshida, Del Angel, & Benítez, ). Focusing on microorganisms also leads to the study of environmental variables that are less evident or relevant at the macroscale, such as the mechanical properties of cell‐to‐cell and cell‐to‐medium interactions (Persat et al, ).…”

Cell‐fate determination in Myxococcus xanthus development: Network dynamics and novel predictions

“…Previous experimental work and dynamic models for M. xanthus have approached cell-fate determination as the result of the differential expression of single genes associated to M. xanthus development (e.g., C-signal; Sozinova et al, 2005Sozinova et al, , 2006Holmes, Kalvala, & Whitworth, 2010). However, some integrative efforts have highlighted the importance of understanding development as the result of interactions among diverse factors (Arias Del Angel et al, 2017;Bretl & Kirby, 2016;Kroos, 2017;Rajagopalan et al, 2014). Nevertheless, these efforts still have not captured the complex dynamics underlying M.…”

“…At the molecular level, M. xanthus development starts with the stringent response triggered by the intracellular accumulation of the molecule (p)ppGpp (Harris, Kaiser, & Singer, 1998). This molecule regulates downstream genes such as the ones coding for the transcription factors Nla's and the actABCD operon (Giglio, Caberoy, Suen, Kaiser, & Garza, 2011;Gronewold & Kaiser, 2001), which in turn allow the expression of at least five signals involved in the coordination and intercellular communication that are crucial to the progression of FB development (Kaiser, 2004;Arias Del Angel et al, 2017;Kroos, 2017). Later in the developmental regulatory process, MrpC, a key transcription factor involved in cellular differentiation towards myxospore, is expressed (Robinson, Son, Kroos, & Kroos, 2014;Sun & Shi, 2001).…”

Complete Genome Sequence of the Fruiting Myxobacterium Myxococcus macrosporus Strain DSM 14697, Generated by PacBio Sequencing

“…Analyses using Myxococcus xanthus as a model organism have provided important insights into regulation of fruiting body formation ( 3 , 4 ). However, comparative genome investigations of different Myxococcales genome sequences have indicated that the developmental program that results in fruiting body formation is not highly conserved ( 5 – 7 ).…”