Microbes at Surface-Air Interfaces: The Metabolic Harnessing of Relative Humidity, Surface Hygroscopicity, and Oligotrophy for Resilience.

Wendy Stone,Jennifer Mckelvie,Gideon M Wolfaardt,Darren R Korber,Otini Kroukamp

doi:10.3389/fmicb.2016.01563

Abstract

The human environment is predominantly not aqueous, and microbes are ubiquitous at the surface-air interfaces with which we interact. Yet microbial studies at surface-air interfaces are largely survival-oriented, whilst microbial metabolism has overwhelmingly been investigated from the perspective of liquid saturation. This study explored microbial survival and metabolism under desiccation, particularly the influence of relative humidity (RH), surface hygroscopicity, and nutrient availability on the interchange between these two phenomena. The combination of a hygroscopic matrix (i.e., clay or 4,000 MW polyethylene glycol) and high RH resulted in persistent measurable microbial metabolism during desiccation. In contrast, no microbial metabolism was detected at (a) hygroscopic interfaces at low RH, and (b) less hygroscopic interfaces (i.e., sand and plastic/glass) at high or low RH. Cell survival was conversely inhibited at high RH and promoted at low RH, irrespective of surface hygroscopicity. Based on this demonstration of metabolic persistence and survival inhibition at high RH, it was proposed that biofilm metabolic rates might inversely influence whole-biofilm resilience, with ‘resilience’ defined in this study as a biofilm’s capacity to recover from desiccation. The concept of whole-biofilm resilience being promoted by oligotrophy was supported in desiccation-tolerant Arthrobacter spp. biofilms, but not in desiccation-sensitive Pseudomonas aeruginosa biofilms. The ability of microbes to interact with surfaces to harness water vapor during desiccation was demonstrated, and potentially to harness oligotrophy (the most ubiquitous natural condition facing microbes) for adaptation to desiccation.

Highlights

Water is widely considered the determining element of the metabolic network that constitutes life on earth (Zolensky, 2005)
The trend of viability inhibition at high relative humidity (RH) remained consistent throughout this study, despite the nature of both the surface and the inoculum
The results from the present study suggest that the RH at soilair interfaces may influence the Birch Effect, with the slower metabolic recovery at high RH, potentially due to the inhibition of microbial viability at high RH (Figures 3 and 6)

Summary

Introduction

Water is widely considered the determining element of the metabolic network that constitutes life on earth (Zolensky, 2005). It is true that microbial activity and survival at surfaceair interfaces must be explored in relation to the essential element water, the study of their activity in these inherently slower desiccated conditions is not anomalous, but rather a truer exploration of how microbes persist and influence many industrial, agricultural, and medical settings relevant to humans Examples of such “slow” surface-air microbiome consequences include the weathering of rock (Gorbushina and Broughton, 2009; de Goffau et al, 2011), structural architecture (Mottershead et al, 2003; Cheng et al, 2016) and artwork (Guglielminetti et al, 1994; Garg et al, 1995), hospital pathogen persistence (Kramer et al, 2006), risk-assessment models for the International Space Station (de Goffau, 2011), solid food contamination (Brown, 1976) and agricultural soil ecology (Stotzky and Pramer, 1972; Ramirez et al, 2004; Ritchie et al, 2006). Microbial diversity has been demonstrated in dust storms (Katra et al, 2014) and microbes can travel great distances whilst maintaining metabolic viability (Meola et al, 2015)

Methods

Results

Conclusion