Quorum sensing control of phosphorus acquisition in Trichodesmium consortia

Abstract

Colonies of the cyanobacterium Trichodesmium are abundant in the oligotrophic ocean, and through their ability to fix both CO 2 and N 2 , have pivotal roles in the cycling of carbon and nitrogen in these highly nutrient-depleted environments. Trichodesmium colonies host complex consortia of epibiotic heterotrophic bacteria, and yet, the regulation of nutrient acquisition by these epibionts is poorly understood. We present evidence that epibiotic bacteria in Trichodesmium consortia use quorum sensing (QS) to regulate the activity of alkaline phosphatases (APases), enzymes used by epibionts in the acquisition of phosphate from dissolved-organic phosphorus molecules. A class of QS molecules, acylated homoserine lactones (AHLs), were produced by cultivated epibionts, and adding these AHLs to wild Trichodesmium colonies collected at sea led to a consistent doubling of APase activity. By contrast, amendments of (S)-4,5-dihydroxy-2,3-pentanedione (DPD)-the precursor to the autoinducer-2 (AI-2) family of universal interspecies signaling molecules-led to the attenuation of APase activity. In addition, colonies collected at sea were found by high performance liquid chromatography/mass spectrometry to contain both AHLs and AI-2. Both types of molecules turned over rapidly, an observation we ascribe to quorum quenching. Our results reveal a complex chemical interplay among epibionts using AHLs and AI-2 to control access to phosphate in dissolved-organic phosphorus.

Quorum Sensing Plays a Complex Role in Regulating the Enzyme Hydrolysis Activity of Microbes Associated with Sinking Particles in the Ocean

“…Hmelo and Van Mooy (2009) observed that AHLs were exceptionally short-lived in natural marine waters, and estimated that only 3-7% of the AHL amendments they made remained after a 24-h incubation period. These results underscore the inherent abiotic chemical instability of AHLs at seawater pH, but also suggest ubiquitous enzymatic degradation (i.e., quorum quenching) in marine environments, which makes capturing natively produced AHLs a challenge (Hmelo and Van Mooy, 2009;Tait et al, 2010;Van Mooy et al, 2012).…”

“…of infochemicals on the activity of particle-associated bacterial assemblages, but they have thus far affirmed that bacterial signaling systems are involved in, and may either enhance or inhibit the rate of the degradation of sinking POC (Hmelo et al, 2011;Van Mooy et al, 2012;Edwards et al, 2015).…”

“…AHLs and other quorum sensing molecules have been observed directly in a wide range of marine environments (Decho et al, 2009;Van Mooy et al, 2012;Zimmer et al, 2014) including sinking particles (Hmelo et al, 2011) and endogenous AHLs are often interpreted to be direct evidence of quorum sensing. We argue that AHLs must truly be dissolved in order to be actively involved in quorum sensing, and therefore sought to identify AHLs present solely in the porewaters of sinking particles by using a solid phase extraction method.…”

“…Hereafter, HPLC vials containing AHL extracts were analyzed via HPLC/MS/MS (Hmelo and Van Mooy, 2009) in order to detect and determine AHLs present in our experiments. An HPLC 1200 Series (Agilent Technologies, MA, USA) connected to a TSQ Vantage triple quadrupole mass spectrometer (TQMS; Thermo Scientific, HB, Germany) was used as described by Van Mooy et al (2012). Data were processed with Excalibur software (Thermo Scientific, HB, Germany).…”

“…Quorum sensing is a cell-density dependent form of communication between microorganisms that involves the secretion of distinct chemical signals in order to coordinate directed behaviors ranging from biofilm formation to antibiotic resistance (Whiteley et al, 1999;Ng and Bassler, 2009). Thus, far, our knowledge about the potential importance of bacterial quorum sensing on sinking particles is limited because only a few cultivation-independent studies have been carried out in the marine environment (Decho et al, 2009;Van Mooy et al, 2012;Ransome et al, 2014;Zimmer et al, 2014;Certner and Vollmer, 2015).…”