Exploring New Horizons Streptomyces Bacteria Employ a Newly-Discovered Cell Type, the "Explorer" Cell, to Rapidly Colonize New Areas in the Face of Competition
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INSIGHT BACTERIA Exploring new horizons Streptomyces bacteria employ a newly-discovered cell type, the "explorer" cell, to rapidly colonize new areas in the face of competition. VINEETHA M ZACHARIA AND MATTHEW F TRAXLER Fla¨rdh, 2012; Fla¨rdh and Buttner 2009). Subse- Related research article Jones SE, Ho L, quently, cells of a third type (spores) form long Rees CA, Hill JE, Nodwell JR, Elliot MA. chains on the ends of these aerial hyphae. These 2017. Streptomyces exploration is triggered spores are resistant to drying out and likely allow Streptomyces to passively spread to new envi- by fungal interactions and volatile signals. ronments through the action of water or air eLife 6:e21738. doi: 10.7554/eLife.21738 movement (McCormick and Fla¨rdh, 2012). Now, in eLife, Marie Elliot at McMaster Univer- sity and colleagues – including Stephanie Jones as first author – report a new form of growth in Streptomyces termed “exploratory growth” istorically, bacteria have been thought (Jones et al., 2016). of as simple cells whose only aim is to In the initial experiments, Jones et al. – who replicate. However, research over the H are based at McMaster University, the University past two decades has revealed that many types of Toronto and Dartmouth College – grew of bacteria are able to develop into communities Streptomyces venezuelae bacteria alone, or that contain several types of cells, with different close to a yeast called Saccharomyces cerevisiae, cell types performing particular roles on solid agar for two weeks. During this time, (Kuchina et al., 2011). These communities are the bacteria grown alone formed a normal sized of interest in scientific fields as diverse as petro- colony typical of Streptomyces. However, in the leum engineering and bacterial pathogenesis. presence of the yeast, the S. venezuelae colonies Streptomyces were perhaps the first bacteria expanded rapidly and colonized the entire sur- to be recognized as having a multicellular life- face of the growth dish, engulfing the nearby style (Waksman and Henrici, 1943). In fact, this yeast colony. In subsequent experiments, the lifestyle led to them being classified as fungi cells produced during exploratory growth when they were first isolated from soil at the (dubbed “explorer” cells) showed the ability to beginning of the last century (Hopwood, 2007). spread over abiotic surfaces including rocks This case of mistaken identity stemmed from the (Figure 1B) and polystyrene barriers. Scanning fuzzy texture of Streptomyces colonies (see electron microscopy revealed that, unlike vege- Figure 1A), which resembles many of the fungi tative cells, these explorer cells did not form we see growing on bread and other natural sur- branches and more closely resembled simple faces (Waksman, 1954). aerial hyphae. The first stage in the life of a Streptomyces Previous studies have identified many genes colony is the growth of so-called vegetative that regulate the development of Streptomyces Copyright Zacharia and Traxler. cells, which form networks of branched filaments colonies including the bld genes, which are This article is distributed under the that penetrate the surfaces of food sources. The involved in the formation of aerial hyphae, and terms of the Creative Commons fuzzy appearance of Streptomyces colonies is the whi genes, which are required to make spores Attribution License, which permits the result of the vegetative cells producing (McCormick and Fla¨rdh, 2012). Jones et al. unrestricted use and redistribution provided that the original author and another type of cell called aerial hyphae that found that neither of these sets of genes are source are credited. grow upwards into the air (McCormick and required for exploratory growth of S. venezuelae Zacharia and Traxler. eLife 2017;6:e23624. DOI: 10.7554/eLife.23624 1 of 3 Insight Bacteria Exploring new horizons Figure 1. The multicellular lifestyle of Streptomyces. Streptomyces bacteria form colonies that contain several different types of specialized cells: vegetative hyphae, aerial hyphae, spores and the "explorer" cells discovered by Jones et al. (A)A Streptomyces coelicolor colony exhibiting aerial hyphae (white) and spores (gray). The blue droplets contain compounds that are naturally produced by S. coelicolor including antibiotics. (B) Streptomyces venezuelae explorer cells spreading on a rock. (C) In addition to these four types of cells, it is possible that Streptomyces colonies might contain other cell types that produce specialized metabolites, such as antibiotics, signaling molecules or volatile organic compounds (VOCs). Image credits: panel A and C Vineetha Zacharia; panel B Jones et al. (2016) in the presence of the yeast. This suggests that Streptomyces displays exploratory growth in the explorer cell type is distinct from the previ- response to shortages of glucose (caused by the ously known developmental pathways in Strepto- presence of the yeast) and to an increased pH in myces. Furthermore, Jones et al. found that the surrounding environment. The bacteria trig- multiple Streptomyces species were capable of ger this pH change themselves by releasing a vol- exploratory growth and that various fungal atile organic compound called trimethylamine, microbes had the ability to trigger this behavior. which is able to stimulate exploratory growth in Further experiments using libraries of mutant Streptomyces over considerable distances. Tri- yeast indicated that glucose and pH may be methylamine also inhibits the growth of other involved in triggering the formation of explorer bacteria that might compete with S. venezuelae cells. Jones et al. demonstrated that in natural environments. Zacharia and Traxler. eLife 2017;6:e23624. DOI: 10.7554/eLife.23624 2 of 3 Insight Bacteria Exploring new horizons The work of Jones et al. opens up the possi- [email protected] bility that there may be additional types of spe- Competing interests: The authors declare that cialized cells within Streptomyces colonies. no competing interests exist. Streptomyces are important for medicine Published 04 January 2017 because they produce many different chemical compounds, including antibiotics and immuno- suppressant drugs, and one might imagine that References specific groups of cells within a colony are Baker ME. 1994. Myxococcus xanthus C-factor, a morphogenetic paracrine signal, is similar to responsible for making these compounds Escherichia coli 3-oxoacyl-[acyl-carrier-protein] (Figure 1C). Perhaps other cell types might be reductase and human 17 beta-hydroxysteroid dedicated to directing the activities of different dehydrogenase. Biochemical Journal 301 (Pt 1):311– cells within the colony (as happens in other bac- 312. doi: 10.1042/bj3010311, PMID: 8037687 teria with multicellular lifestyles; Lopez et al., Fla¨ rdh K, Buttner MJ. 2009. Streptomyces morphogenetics: dissecting differentiation in a 2009; Baker, 1994), perhaps by producing tri- filamentous bacterium. Nature Reviews Microbiology methylamine or other volatile organic 7:36–49. doi: 10.1038/nrmicro1968, PMID: 19079351 compounds. Hopwood DA. 2007. Streptomyces in Nature and For decades, researchers have described Medicine: The Antibiotic Makers. Oxford, New York: Streptomyces colonies in terms of vegetative Oxford University Press. p. 250 Jones SE, Ho L, Rees CA, Hill JE, Nodwell JR, Elliot cells, aerial hyphae and spores. The explorer cells MA. 2017. Streptomyces exploration is triggered by identified by Jones et al. offer Streptomyces an fungal interactions and volatile signals. eLife 6:e21738. alternative means of escape from their normal life doi: 10.7554/eLife.21738 cycle and local environment in the face of compe- Kuchina A, Espinar L, C¸ag˘atay T, Balbin AO, Zhang F, tition. This makes intuitive sense, given that Alvarado A, Garcia-Ojalvo J, Su¨ el GM. 2011. Temporal competition between differentiation programs Streptomyces lack the ability to move (“motility”) determines cell fate choice. Molecular Systems Biology in the traditional sense (for example, by swim- 7:557. doi: 10.1038/msb.2011.88, PMID: 22146301 ming, gliding or twitching). Taken together, the Lo´ pez D, Vlamakis H, Losick R, Kolter R. 2009. work of Jones et al. demonstrates a surprisingly Paracrine signaling in a bacterium. Genes & dynamic strategy in which a ‘non-motile’ bacte- Development 23:1631–1638. doi: 10.1101/gad. 1813709, PMID: 19605685 rium can use cues from other microbes, long- McCormick JR, Fla¨ rdh K. 2012. Signals and regulators range signaling, and multicellularity to make a that govern Streptomyces development. FEMS graceful exit when times get tough. Microbiology Reviews 36:206–231. doi: 10.1111/j. 1574-6976.2011.00317.x, PMID: 22092088 Vineetha M Zacharia is in the Department of Waksman SA, Henrici AT. 1943. The nomenclature Plant and Microbial Biology, University of and classification of the Actinomycetes. Journal of Bacteriology 46:337–341. PMID: 16560709 California, Berkeley, Berkeley, United States Matthew F Traxler Waksman SA. 1954. My Life with the Microbes. New is in the Department of Plant York: Simon and Schuster. p. 364 and Microbial Biology, University of California, Berkeley, Berkeley, United States Zacharia and Traxler. eLife 2017;6:e23624. DOI: 10.7554/eLife.23624 3 of 3.