Controlling the Microbiome: Microhabitat Adjustments for Successful Biocontrol Strategies in Soil and Human Gut

摘要

Introduction The human gut and the rhizosphere are environments colonized by highly diverse communities of microbes, which perform complex interactions with their host and carry out important functions including enhanced disease resistance and nutrient uptake. In humans they are involved in energy harvest and storage as well as in interactions with the immune system (Clemente et al., 2012 ). In plants they have profound effects on seed germination, seedling vigor, nutrition, plant health, and development of the innate immune system (Mendes et al., 2013 ; Berg et al., 2014a ; Schikora et al., 2016 ). The composition of the microbial communities is host-specific and related to its health status (Smalla et al., 2001 ; Kinross et al., 2011 ; Berg et al., 2014a ). Imbalances caused by disturbance-induced shifts in microbial species abundances can lead to disease outbreaks in both environments (Berendsen et al., 2012 ; Robles Alonso and Guarner, 2013 ; Berg et al., 2014b ) and further to probable proliferation of pathogenic species (Van Elsas et al., 2012 ; Van Agtmaal et al., 2015 ).To restore or maintain the health of the host, bio-based solutions supporting the pathogen-suppressing ability of the hosts' native microbiome can be applied, including probiotics, synbiotics and biocontrol agents (de Vrese and Schrezenmeir, 2008 ). Such methods aim to increase the abundance and activity of host beneficial bacteria (HBB). However, addition of HBB does not always result in the desired pathogen suppression due to insufficient establishment, i.e., lower survival and/or poor colonization rates of the HBB (Bashan et al., 2014 ).Concepts from invasion ecology suggest that survival rates of invaders are inversely related to the diversity of the native microbiome. This can be explained by higher resource uptake and consequent reduction in niche availability (Mallon et al., 2015 ). In addition, prevailing physical and chemical parameters in the respective environment like texture, pore size distribution, and moisture content might not favor the establishment of the introduced HBB. For a long-term establishment of the HBB in the soil these abiotic factors have to be considered. In the gut, the colonization resistance determined by the commensal microbiome is linked to its capacity to exploit the available niches and to prevent the establishment of invaders via niche occupation (reviewed in Stecher et al., 2013 ). The knowledge on mechanisms of microbial invasions (Mallon et al., 2015 ) can be used to improve the survival of HBB in both environments.Given that similar mechanisms drive microbial colonization and establishment in the gut and rhizosphere microbiomes, we suggest that biocontrol strategies could be similar for both environments (Ramírez-Puebla et al., 2013 ; Berg et al., 2015 ; Mendes and Raaijmakers, 2015 ). Here we develop possible strategies to ensure long-term establishment of HBB by manipulating niche availability. Creating microhabitats for host beneficial bacteria by introducing minor disturbances Several studies have shown that soils harboring low microbial biomass or low microbial diversity are more susceptible to colonization by other organisms (Flie?bach et al., 2009 ; Van Elsas et al., 2012 ). Certain agricultural practices can result in major disturbances of the rhizosphere microbiome . Examples include disinfestation with chemical pesticides, heat treatment (Stapleton, 2000 ), radiation or anaerobic disinfestation (Van Agtmaal et al., 2015 ). Moreover, tillage systems may have major effects on the established community by reducing certain soil microbial populations, particularly fungi (Ventorino et al., 2012 ). Analogous events, leading to changes in the human gut microbiome , are the application of broad spectrum antibiotics, fecal transplantations (Landy et al., 2011 ; de Vos, 2013 ) or considerable changes in diet (Turnbaugh et al., 2009 ). Whilst major disturbances are frequently used to eliminate pathogens, those methods possibly also disrupt beneficial functions of the indigenous microbial community (Altieri, 1999 ; Geiger et al., 2010 ).An alternative strategy is to introduce minor disturbances to create free niches for HBB's in both the rhizosphere and the human gut microbiome. This strategy aims to selectively empty niches in the existing community.In the rhizosphere the introduction of accessory bacterial predators such as protozoa (e.g., flagellates, ciliates) or nematodes (Jousset et al., 2006 ; Abada et al., 2009 ; Pedersen et al., 2009 ; Freyth et al., 2010 ; Neidig et al., 2011 ; Müller et al., 2013 ) could foster biocontrol strains via enhanced selective predation when the biocontrol strain protects itself through production of antibiotics. The increase in predation pressure might also stimulate biocontrol strategies by direct predation on pathogens as well as nutrient turnover and bacterial activity in soil. Likewise, specific bacteriophages could be applied to selectively eliminate t