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Hierarchical Evolution of the Bacterial Sporulation Network View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Current Biology 20, R735–R745, September 14, 2010 ª2010 Elsevier Ltd All rights reserved DOI 10.1016/j.cub.2010.06.031 Hierarchical Evolution of the Bacterial Review Sporulation Network Michiel J.L. de Hoon1,y, Patrick Eichenberger2, In metazoans, studies at the interface of evolution and devel- and Dennis Vitkup1,3 opment investigate the mechanistic changes leading to the organization and evolution of complex body plans. On the basis of careful analyses of several model systems, such Genome sequencing of multiple species makes it possible as Drosophila and sea urchin, the essential role of regulatory to understand the main principles behind the evolution interactions in the evolution of developmental processes has of developmental regulatory networks. It is especially been firmly established [5,6]. interesting to analyze the evolution of well-defined model Although prokaryotic organisms do not have a complex systems in which conservation patterns can be directly body plan, they can form multi-cellular structures, such as correlated with the functional roles of various network biofilms and fruiting bodies [7,8]. In addition, elaborate components. Endospore formation (sporulation), exten- developmental processes have been characterized in many sively studied in Bacillus subtilis, is driven by such a model bacterial species. Endospore formation (sporulation) is the bacterial network of cellular development and differentia- prime example of a complex bacterial developmental pro- tion. In this review, we analyze the evolution of the sporu- cess. Sporulating bacteria undergo an intricate sequence lation network in multiple endospore-forming bacteria. of cell differentiation events leading to the formation of a Importantly, the network evolution is not random but highly resistant, dormant spore that can germinate when primarily follows the hierarchical organization and func- conditions improve. Initiation and progression of sporulation tional logic of the sporulation process. Specifically, the is controlled by a complex network of protein–protein and sporulation sigma factors and the master regulator of protein–DNA interactions, consisting of regulatory modules, sporulation, Spo0A, are conserved in all considered spore- signaling pathways, feed-forward network motifs, and post- formers. The sequential activation of these global regula- translational regulation [8–10]. tors is also strongly conserved. The feed-forward loops, The sporulation process has been characterized in suffi- which are likely used to fine-tune waves of gene expres- cient detail in the model organism Bacillus subtilis to enable sion within regulatory modules, show an intermediate level fundamental evolutionary analyses from a functional per- of conservation. These loops are less conserved than the spective. Similar to developmental processes in higher sigma factors but significantly more than the structural organisms, bacterial sporulation is governed by a complex sporulation genes, which form the lowest level in the cascade of regulatory interactions that contains a strongly functional and evolutionary hierarchy of the sporulation conserved regulatory kernel, i.e. core regulatory network network. Interestingly, in spore-forming bacteria, gene [11]. Transcriptional regulation in the sporulation network is regulation is more conserved than gene presence for dominated by sigma factors — the subunit of the bacterial sporulation genes, while the opposite is true for non-spor- RNA polymerase holoenzyme that is responsible for recog- ulation genes. The observed patterns suggest that, by nizing promoter regions on the DNA [12]. The DNA-binding understanding the functional organization of a develop- specificities of different sigma factors have been determined mental network in a model organism, it is possible to experimentally and the corresponding DNA-binding sites understand the logic behind the evolution of this network have been collected in DBTBS, the database of transcrip- in multiple related species. tional regulation in B. subtilis [13]. The rapid increase in fully sequenced bacterial genomes allows us to understand the evolution of network regulation Introduction in a large number of diverged species. In this review, we first Evolution is the main organizational principle of biological present an overview of the well-studied sequence of sporu- systems [1,2]. The emerging field of evolutionary systems lation events in B. subtilis. Next, we describe the phyloge- biology [3,4] investigates structural and functional evolution netic relationships of currently sequenced endospore-form- of cellular networks. Instead of considering only the pres- ing bacteria. We follow with a discussion of the evolution of ence or absence of orthologous genes in sequenced organ- the sporulation gene regulatory network and the properties isms, evolutionary systems biology primarily focuses on affecting the evolvability of regulation. The functional char- changes in the relationships between genes and their acterization of a substantial fraction of sporulation genes in products. A thriving area of evolutionary systems biology B. subtilis enables us to put the observed evolutionary is the evolutionary biology of developmental networks. patterns into the proper functional context. We also discuss the correlation between evolution of gene presence and regulation. 1Center for Computational Biology and Bioinformatics, Columbia University, New York, NY 10032, USA. 2Center for Genomics and The Sporulation Process and Its Regulation in B. subtilis Systems Biology, Department of Biology, New York University, New The genetically competent, non-pathogenic soil bacterium York, NY 10003, USA. 3Department of Biomedical Informatics, B. subtilis is the prevalent model system for studies of spor- Columbia University, New York, NY 10032, USA. yCurrently at the ulation. A significant amount of detailed molecular data has RIKEN Omics Science Center, 1-7-22 Suehiro-cho, Tsurumi-ku, been gathered over the years to characterize the mechanism Yokohama City, Kanagawa, 230-0045, Japan. of endospore formation — in particular, the regulation of the E-mail: [email protected] (P.E.), [email protected] (D.V.) different sporulation stages. Current Biology Vol 20 No 17 R736 Figure 1. Morphological stages of the σA B. subtilis life cycle. The temporal and compartment-specific Vegetative growth activity of each sporulation sigma (s) factor A A σ σ σA is indicated. During vegetative growth, cells Binary fission divide by binary fission to generate two iden- σA tical daughter cells. Sporulation is initiated in response to starvation. In the predivisional sporulating cell, the chromosomes (red) are Germination Initiation of sporulation oriented with their origin-proximal region σH anchored at the cell poles. During asymmetric division, two membrane-bounded compart- ments are generated: a small forespore and a large mother cell. After asymmetric division, Spore release Asymmetric division the remainder of the forespore chromosome (i.e. the origin-distal region) is pulled into the forespore by translocation. Engulfment of the forespore by the mother cell results in the release of the forespore as a free proto- σF plast in the mother cell. The cortex (com- posed of modified peptidoglycan, gray) is Mother cell lysis Engulfment synthesized between the two membranes surrounding the forespore. The coat (black) is a complex structure made of at least 70 Coat formation distinct proteins that assemble around the σK σE forespore surface. Following mother cell lysis, G σ Cortex formation the mature spore is released into the environ- ment. B. subtilis cells can remain in a dormant Current Biology spore state for an extended period of time, but spores will germinate in response to the presence of small molecules (e.g. single amino acids, sugars or fragments of peptido- glycan) and resume vegetative growth. Morphological Stages of Sporulation and Formation region) is captured in the small chamber of the dividing of Protective Structures cell. A DNA translocase, SpoIIIE, located at the center of In rich medium, B. subtilis cells divide by binary fission the polar septum, is necessary to pull the rest of this chromo- approximately every 30 minutes. By contrast, deterioration some into the forespore [21–23]. The other chromosome is of environmental conditions triggers sporulation, a develop- localized entirely inside the mother cell. mental process that takes about 8 to 10 hours. Thus, endo- Following asymmetric division, the next morphological spore formation represents a formidable investment of time stage of sporulation is the engulfment of the forespore by and energy and is considered to be a survival pathway of the mother cell. This process is analogous to phagocytosis last resort, as B. subtilis cells only commit to sporulation and is driven by mother cell proteins that facilitate membrane after they failed to deal with starvation in other ways, such migration around the forespore by enzymatic removal of the as cannibalism or establishment of a genetically competent peptidoglycan [24,25]. After completion of engulfment, the state [14–16]. The successive morphological stages of spor- forespore, now entirely surrounded by its inner and outer ulation have been defined using electron microscopy [17,18] membranes, is a free protoplast in the mother cell cytoplasm. (Figure 1). Sporulation begins with an asymmetric cell divi-
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