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Quorum Sensing in Extreme Environments

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Quorum Sensing in Extreme Environments Life 2013, 3, 131-148; doi:10.3390/life3010131 OPEN ACCESS life ISSN 2075-1729 www.mdpi.com/journal/life Review Quorum Sensing in Extreme Environments Kate Montgomery 1, James C. Charlesworth 1, Rebecca LeBard 1, Pieter T. Visscher 2, 3 and Brendan P. Burns 1,3,* 1 School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW 2052, Australia; E-Mails: [email protected] (K.M.); [email protected] (J.C.C.); [email protected] (R.L.) 2 Center for Integrative Geosciences, University of Connecticut 354 Mansfield Road, Storrs, CT 06269-2045, USA; E-Mail: [email protected] 3 Australian Centre for Astrobiology, University of New South Wales, Sydney, NSW 2052, Australia * Author to whom correspondence should be addressed; E-Mail: [email protected]; Tel.: +61-2-9385-3659; Fax: +61-2-9385-1591. Received: 10 December 2012; in revised form: 21 January 2013 / Accepted: 22 January 2013 / Published: 29 January 2013 Abstract: Microbial communication, particularly that of quorum sensing, plays an important role in regulating gene expression in a range of organisms. Although this phenomenon has been well studied in relation to, for example, virulence gene regulation, the focus of this article is to review our understanding of the role of microbial communication in extreme environments. Cell signaling regulates many important microbial processes and may play a pivotal role in driving microbial functional diversity and ultimately ecosystem function in extreme environments. Several recent studies have characterized cell signaling in modern analogs to early Earth communities (microbial mats), and characterization of cell signaling systems in these communities may provide unique insights in understanding the microbial interactions involved in function and survival in extreme environments. Cell signaling is a fundamental process that may have co-evolved with communities and environmental conditions on the early Earth. Without cell signaling, evolutionary pressures may have even resulted in the extinction rather than evolution of certain microbial groups. One of the biggest challenges in extremophile biology is understanding how and why some microbial functional groups are located where logically they would not be expected to survive, and tightly regulated communication may be key. Finally, quorum sensing has been recently identified for the first time in archaea, and thus communication at multiple levels (potentially even inter-domain) may be fundamental in extreme environments. Life 2013, 3 132 Keywords: quorum sensing; extremophiles; microbial communication 1. Introduction Quorum sensing is a type of microbial communication that regulates gene expression in high cell densities [1]. It relies on the production of signaling molecules that are released from the cell into the surrounding environment. Each cell produces these molecules constitutively, and it is when they reach a critical concentration that gene transcription is initiated. Quorum sensing is considered to be a process by which the microbial population as a whole can monitor and regulate gene expression and hence physiology (including metabolism), as the characteristics controlled by quorum sensing are unproductive when undertaken by a single cell alone [1±3]. Quorum sensing is known to be responsible for the regulation of bioluminescence, cell competency and horizontal gene transfer, virulence, motility, the formation of biofilms and the production of antibiotics and other secondary metabolites [4,5]. A number of quorum sensing systems have now been well characterized and extensively documented, such as those that regulate the production of bioluminescence in the marine bacteria Vibrio harveyi and Allivibrio fischeri [1,6]. There still remains a wide range of organisms and environments in which quorum sensing has yet to be identified or characterized, with extremophiles being one of these groups of organisms. The extremophiles represent a variety of organisms known for their ability to survive in and adapt to ³extreme´ environmental conditions [7]. Though this is an anthropogenic definition, organisms in this group demonstrate the breadth of environments that life can survive in. This includes high and low pH levels, extremes of hot and cold, high-pressure levels, salinity (high and low), nutrient limitations, or combinations of the above. Short-term fluctuations in environmental parameters can also be considered as an extreme condition, as microorganisms need to be able to rapidly adapt to survive in a given niche. This is particularly relevant in an environment of interest, microbial mats, to be covered later in this review. Extremophiles have been studied intensively in recent years for their insight into environmental adaptation. Of particular interest for researchers is the potential for application of extremophilic metabolites and extracellular enzymes in industry and biotechnology as demands in these areas increase [8]. The role of quorum sensing in extreme environments is one not currently investigated in detail. The importance of quorum sensing in the adaptation of microorganisms in general, and particularly ³extremophiles´ to their environment has been studied in a limited number of individual organisms, however the role of quorum sensing in the extended microbial biosphere is still relatively unknown. The advent of bioinformatic technologies and extensive databases has allowed for a relative wealth of information regarding the extremophiles. As they live in such harsh conditions culturing in the laboratory is often difficult, though not impossible. Consequently, it has been largely the recent ability to perform genomic and proteomic studies on environmental samples that has allowed considerable insight into the capabilities of these microbes. This review aims to assess our current understanding of quorum sensing in extreme environments and present the evidence for its potential role and function in these ecosystems. Life 2013, 3 133 2. Quorum Sensing Systems Quorum sensing was first identified in the organisms V. harveyi and A. fischeri that were noted to produce a luminescent quality when cells reached a particular level of density. These and other Gram-negative bacteria were found to have a common genetic system that is known as the LuxI-LuxR, or AI-1, quorum sensing system. From these initial observations a second more universal sensing system was identified, though whether it is a true signaling system is a source of debate. This is the autoinducer-2 (AI-2) system [1,3,6]. The LuxI-LuxR system as observed in the Vibrio spp. makes use of acylated homoserine lactones (AHLs) as autoinducers. It is these molecules that are released and received in this quorum sensing system. AHL-based signaling has now been identified in more than 70 microbial species [2,3]. Interestingly while this system was first observed in the proteobacterial phylum, it has been recently identified in cyanobacteria [9] and most recently within archaea [10]. AHLs are produced by the LuxI synthase or its homologue. AHLs all contain a central ring structure that remains constant, but they differ considerably in their side-chains. These vary in length and may possess oxo or hydroxyl groups, allowing the signaling molecules to be species specific [2]. The molecules exit and re-enter the cells by either active transport or passive diffusion depending on the size of the molecule and environmental conditions. The chemical properties of the AHL side chain (e.g., the number of carbon atoms in the alkyl side chain), has a profound impact on signaling efficiency. The stability of long chain alkyl groups (e.g., C10±C14) at elevated pH (> 8.2) is several orders of magnitude greater than that of short chain ones. This suggests that changing ratios of short and long chain sides (caused by the pH of the environment) can be used by cells to determine this physicochemical value. When extracellular concentrations of the signals reach a critical level, the AHLs bind to the lux box, a promoter element, resulting in transcription of the associated genes [11]. Interestingly AHLs have been shown to readily degrade under high temperatures and alkaline pH conditions, with the lactone ring coming under nucleophilic attack. This lactone ring has the capability of reforming if the pH is lowered substantially to a pH of 2.0 [12]. Longer chain AHLs appear to be more resistant to chemical degradation and as such may be utilized by microbes that live in harsher conditions [12,13]. Furthermore, the stability of long chain alkyl groups (e.g., C10±C14) at elevated pH (> 8.2) is several orders of magnitude greater than that of short chain alkyl groups. By detecting a change in the ratio between long and short chain AHLs, microorganisms may be able to determine the actual pH of their environment. This mechanism has been proposed for microbial mats that are discussed in a later section. Unlike the signaling molecules found in the LuxI-LuxR system, the autoinducer molecules utilized in AI-2 quorum sensing system are all identical [14]. This has led to the suggestion that the AI-2 quorum sensing system is a universal system, allowing both inter- and intra-species communication. The AI-2 system is moderated by the luxS gene that encodes for S-ribosyl homocysteine lyase, a Fe2+ dependent enzyme that cleaves bonds in the S-ribosylhomocysteine (SRH) to produce the precursors to AI-2 signals. The function of the AI-2 signal varies and depends on the associated genes [5]. The autoinducer 2 or AI-2 system that utilizes furanosyl borate diesters as a messenger molecule was initially described as a bacterial ³Esperanto´ or universal language, due to ubiquitous nature of luxS, the protein that synthesizes the diesters [15]. However, this idea however has been criticized as it is uncertain whether the diesters are indeed acting as signaling molecules in all instances. The luxS gene Life 2013, 3 134 is a part of a biochemical pathway that recycles S-adenosyl-L-methionine, and as such, it is possible the AI-2 molecule is merely a byproduct rather than a true signal [16].
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