The ecology of transfer of mobile genetic elements

Abstract

The ecological aspects of the transfer and spread of mobile genetic elements (MGE) are reviewed in the context of the emerging evidence for the dominant role that horizontal gene transfer (HGT) has played in the evolutionary shaping of bacterial communities. Novel tools are described that allow a refined analysis of HGT in natural settings. The occurrence of HGT processes in soil and water, as affected by environmental factors, is then discussed. Examples are provided that illustrate how MGE can influence the behavior of microorganisms in their natural habitats. The occurrence of microorganisms as groups of cells in structured communities, such as those found in biofilms, is used as a framework in order to review the data and pose further questions on the evolutionary role and significance of contemporary gene transfer processes in nature. Selection by the environment is likely to be the dominant force in shaping the genetic make-up of bacterial communities. In fact, selective force can act as an apparent accelerator of gene transfer processes, mainly as a result of the enhancement of survival and persistence of favorably selected products of gene transfer processes (genes, metabolic pathways, microbial cells and communities). However, the current understanding of the triggering and impact of HGT in nature remains limited by our lack of understanding of the very nature and variety of the selective forces that act on microorganisms in situ. Hence, the relevant questions with respect to these triggers acting in natural habitats need to be answered using advanced approaches for studying HGT processes in nature, such as those discussed in this review.

Spatial structure and nutrients promote invasion of IncP-1 plasmids in bacterial populations

“…This is consistent with observations that spatially structured, nutrient-rich habitats, such as the gastrointestinal tract, manure-treated soils, wastewater treatment plants, rhizo-and phylosphere and other surfaces that occasionally receive high supplies of nutrients, are hotspots for horizontal gene transfer (van Elsas and Bailey, 2002). For planktonic bacteria, the chance of contacting another bacterial cell is rare, unless cells densities are high (410 10 c.f.u.…”

“…Plasmids play an important role in the evolution and rapid adaptation of bacteria and archaea by spreading multidrug resistance and many other traits among distantly related hosts (Mazodier and Davies, 1991;Drö ge et al, 1999;van Elsas and Bailey, 2002;Smets and Barkay, 2005;Sørensen et al, 2005;Thomas and Nielsen, 2005). In spite of their importance in bacterial adaptation, we currently have a poor understanding of the population dynamics of plasmids in the absence of selection for the traits they encode.…”

“…Hypotheses have been raised about possible plasmid transfer inhibition mechanisms, or the lack of nutrient availability in those deeper cell layers. Nutrients have been shown to positively affect plasmid transfer efficiency in some cases, but not in others (Hausner and Wuertz, 1999;van Elsas and Bailey, 2002), and therefore it remains unclear why a plasmid does not completely invade a colony or biofilm, and if specific conditions may be conducive to plasmid invasion (Licht et al, 1999;Molin and Tolker-Nielsen, 2003).…”

Influence of industrial contamination on mobile genetic elements: class 1 integron abundance and gene cassette structure in aquatic bacterial communities

“…Previous approaches to examine the role of horizontal gene transfer in microbial evolution have involved the use of a comparative approach to reconstruct historical gene transfer events (for example, Boucher et al, 2003;Kunin et al, 2005;Comas et al, 2006;Doolittle and Bapteste, 2007), the use of in vivo or in vitro gene transfer experiments where gene transfer rates are estimated under controlled conditions (for example, Dahlberg et al, 1998;van Elsas and Bailey, 2002) or molecular investigations of cellular regulation and machinery involved in the process (for example, Thorsted et al, 1998;Lambertsen et al, 2004). While these methods have merit for revealing evolutionary relationships among organisms and the mechanisms that lead to transfer, they rarely reflect in situ gene transfer potential in microbial assemblages.…”

“…Several studies have detected MGEs including plasmids, transposons and integrons across a wide variety of habitats (for example, Sobecky, 1999;Smalla and Sobecky, 2002;van Elsas and Bailey, 2002;Frost et al, 2005), but rarely in a quantitative manner due to previous methodological constraints. In those studies that did quantify MGE abundance in bacterial communities, class 1 integrase (intI1) genes were shown to be abundant in Gram-positive and Gram-negative bacteria in poultry litter obtained from farms with varying antibiotic usage regimes regardless of antibiotic usage (Nandi et al, 2004), while mercury exposure was recently demonstrated to increase the abundance of IncP-1 plasmids (Smalla et al, 2006).…”