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Autoinducers Extracted from Microbial Mats Reveal a Surprising Diversity of N-Acylhomoserine Lactones (Ahls) and Abundance Changes That May Relate to Diel Ph

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Autoinducers Extracted from Microbial Mats Reveal a Surprising Diversity of N-Acylhomoserine Lactones (Ahls) and Abundance Changes That May Relate to Diel Ph Environmental Microbiology (2009) 11(2), 409–420 doi:10.1111/j.1462-2920.2008.01780.x Autoinducers extracted from microbial mats reveal a surprising diversity of N-acylhomoserine lactones (AHLs) and abundance changes that may relate to diel pH Alan W. Decho,1* Pieter T. Visscher,2 John Ferry,3 or night-time incubations revealed that accumulations 1 3 Tomohiro Kawaguchi, Lijian He, of extractable shorter-chain AHLs (e.g. C8- and 2 1 Kristen M. Przekop, R. Sean Norman and C10-AHLs) were significantly (P < 0.001) diminished R. Pamela Reid4 during daytime. Our study offers evidence that stabili- 1Department of Environmental Health Sciences, Arnold ties of AHLs under natural conditions may be influ- School of Public Health, and 3Department of Chemistry enced by the proximal extracellular environment. and Biochemistry, College of Arts and Sciences, We further propose that the ancient periodicity of University of South Carolina, Columbia, SC 29208, photosynthesis/respiration in mats may potentially USA. drive a mechanism for diel differences in activities of 2Department of Marine Sciences, University of certain autoinducers, and hence bacterial activities Connecticut, 1084 Shennecossett Rd., Groton, mediated through quorum sensing. CT 06340-6097, USA. 4Division of Marine Geology and Geophysics, Rosenstiel Introduction School of Marine and Atmospheric Sciences, University of Miami, 4600 Rickenbacker Causeway, Miami, Quorum sensing (QS) is a form of microbial chemical FL 33149-1098, USA. communication that relies on the production and release of molecular signals into the extracellular environment, and their subsequent concentration-dependent detection Summary by proximal cells resulting in gene modulation (Fuqua Microbial mats are highly structured and diverse com- et al., 1996; Fuqua and Greenberg, 2002). Bacteria are munities, and one of the earliest-known life assem- now known to employ a range of small molecules as blages. Mat bacteria interact within an environment signals (Camilli and Bassler, 2006). marked by strong geochemical gradients and fluctua- The N-acylhomoserine lactones (AHLs) are a highly tions. We examined natural mat systems for the pres- conserved class of QS signals used by a wide range of ence of autoinducers involved in quorum sensing, a Gram-negative proteobacteria (Fuqua et al., 2001). They form of cell–cell communication. Our results revealed consist of a five-member homoserine lactone with an that a diverse array of N-acylhomoserine lactones amide-linked acylated side-chain (Fuqua et al., 2001; (AHLs) including C4-toC14-AHLs, were identified from Miller and Bassler, 2001; Waters and Bassler, 2005). mat extracts using mass spectrometry (MS), with When bacteria are present in high local abundances AHLs further confirmation by MS/MS-collision-induced dis- may accumulate to high concentrations (e.g. nM to mM) sociation (CID), and additions of external standards. externally, and upon reaching a threshold concentration Microelectrode measurements showed that mats (nM) within cells form a complex with a regulator protein exhibited diel pH fluctuations, ranging from alkaline that induces changes in gene expression (Hanzelka and (pH 9.4) during daytime (net photosynthesis) to Greenberg, 1995). Laboratory culture studies have shown acidic (pH 6.8) during darkness (net respiration/ over 70 different species of bacteria that produce AHLs fermentation). Under laboratory conditions, AHLs (Waters and Bassler, 2005), and the presence of com- having shorter acyl-chains were degraded within the plete QS circuits in 68 different bacterial genomes (Case time frame that daily alkaline pH (> 8.2) conditions et al., 2008) that have been sequenced thus far. To date, exist in mats. Intensive sampling of mats after full day- AHLs have not been found in Archaea. Quorum sensing is thought to occur within bacterial communities under a range of natural conditions (Horswill Received 19 May, 2008; accepted 7 August, 2008. *For correspon- dence. E-mail [email protected]; Tel. (+1) 803 777 6584; et al., 2007). While a great deal has been learned from Fax (+1) 803 777 3391. laboratory studies concerning the molecular mechanisms Journal compilation © 2008 Society for Applied Microbiology and Blackwell Publishing Ltd No claim to original US government works 410 A. W. Decho et al. of QS, comparatively little has been understood regarding tions of autotrophic production by cyanobacteria and AHLs and their functions in natural systems (McLean heterotrophy, notably the SRB (Reid et al., 2000; Visscher et al., 1997; Bachofen and Schenk, 1998; Miller et al., et al., 2000). The Type-2 stromatolite mats (used in our 2005; Horswill et al., 2007). During their movement study) contain an EPS-rich heterotrophic biofilm on their through the extracellular environment [via diffusion or lipid surface that is underlain by a dense layer of cyanobacte- vesicle carriers (Mashburn and Whiteley, 2005)] to neigh- ria, and exhibit precipitation of a microcrystalline layer of bouring cells the physical/chemical integrity of signals calcium carbonate (i.e. laminae). may be compromised by rapidly changing geochemical/ Herein, the mat environments of marine stromatolites photochemical variables. An important step in assessing (Fig. 1) were examined for the presence and activities of the relevance of bacterial signalling under natural AHLs in QS, and to assess how certain geochemical conditions will be in understanding the persistence and changes such as pH may influence their stability and modifications of signals within the ‘in situ’ extracellular accumulation. We specifically focused on the lithifying environments of microbiota. Type-2 mats for extractions of autoinducers because of Microbial mats are complex assemblages of spatially their relatively high cell abundances and activities. organized bacteria from different functional groups (Des Marais, 1990), and represent one of the earliest life ass- Results and discussion emblages extending 3.4–3.5 Gy bp (Shen et al., 2001; Tice and Lowe, 2004; Allwood et al., 2006; Canfield, Interactions among mat bacteria are likely complex, but 2006). Mats display the highest metabolic rates docu- poorly understood and occur within an environment mented, and have had a substantial impact on the evolu- marked by strong environmental fluctuations. Quorum tion of the Earth (Canfield et al., 2000; Jørgensen, 2000). sensing is a fundamental interaction among bacteria These laminated, organo-sedimentary biofilms typically (Fuqua et al., 1996). Our results revealed that a diverse exhibit tightly coupled cycles of photosynthetic production range of AHL autoinducers were extractable from natural and heterotrophic consumption (Des Marais, 1990) and microbial mats. The AHLs included C4-, C6-, oxo-C6-, C7-, sharp geochemical gradients over small (mmtomm) C8-, oxo-C8-, C10-, C12- and C14-AHLs, and were detect- spatial scales. The high diversities, abundances and able from mat extracts using mass spectrometry (MS). activities of cells within the different functional groups of This represents the first (to our knowledge) extractions mat communities (Ley et al., 2006; Feazel et al., 2008) and specific identifications of AHLs from microbial mats. present an ideal platform for initiating studies of QS in Diel cycling within the mat environment appeared to sig- natural systems. nificantly reduce the relative abundances of certain AHLs, Earlier studies showed that the structural integrity of through alkaline pH lactonolysis. This result was sup- AHLs was susceptible to alkaline conditions (Voelkert ported by concurrent geochemical measurements of pH in and Grant, 1970; Yates et al., 2002). Photosynthetically natural mats over a diel cycle, and by laboratory experi- dominated mat environments are characterized by sharp ments of pH-mediated AHL degradation. geochemical (e.g. pH, O2) gradients, which fluctuate between acidic and alkaline conditions over a diel (i.e. Characterizations of AHLs 24 h) cycle (Des Marais, 1990; Visscher and van Gemer- den, 1991). Hence, the strong fluctuations in pH that Extractions using dichloromethane (DCM), and subse- typically occur in mat environments may represent a quent purification by LC/MS (i.e. liquid chromatography/ substantial constraint to AHL-mediated QS. mass spectrometry) (Fig. 2) revealed putative AHLs Marine stromatolites are a type of laminated, lithifying having retention times and a mass/charge (m/z) corre- microbial mat (Grotzinger and Knoll, 1999). The mats are sponding to AHL standards (Morin et al., 2003). In-source composed of five major functional groups of bacteria: collision-induced dissociation (CID) was used for further cyanobacteria, sulfate reducers [sulfate-reducing bacteria spectral interpretation. Selectivity was based on the (SRB)], fermenters, aerobic heterotrophs, sulfur oxidizers MS/MS fragmentation of the molecular [M+H]+ ions, and (Reid et al., 2000), and the Archaea (R.S. Norman, on their relative intensities. Upon CID, the protonated unpublished). Together, the bacterial functional groups precursor form of each AHL gave rise to the characteristic form three distinct microbial mat communities, termed product ion m/z 102, a protonated homoserine lactone Types 1, 2 and 3 (Reid et al., 2000). Repeated cycling of (Morin et al., 2003). Subsequent MS/MS fragmentation the three communities results in newly lithified layers (i.e. patterns of individual peaks corresponded to C4-, C6-, laminae), and ultimately, the upward growth of the stro- oxo-C6-, C7-, C8-, oxo-C8-, C10-, C12- and C14-AHLs matolite structure
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