Detecting rare gene transfer events in bacterial populations

Abstract

Horizontal gene transfer (HGT) enables bacteria to access, share, and recombine genetic variation, resulting in genetic diversity that cannot be obtained through mutational processes alone. In most cases, the observation of evolutionary successful HGT events relies on the outcome of initially rare events that lead to novel functions in the new host, and that exhibit a positive effect on host fitness. Conversely, the large majority of HGT events occurring in bacterial populations will go undetected due to lack of replication success of transformants. Moreover, other HGT events that would be highly beneficial to new hosts can fail to ensue due to lack of physical proximity to the donor organism, lack of a suitable gene transfer mechanism, genetic compatibility, and stochasticity in tempo-spatial occurrence. Experimental attempts to detect HGT events in bacterial populations have typically focused on the transformed cells or their immediate offspring. However, rare HGT events occurring in large and structured populations are unlikely to reach relative population sizes that will allow their immediate identification; the exception being the unusually strong positive selection conferred by antibiotics. Most HGT events are not expected to alter the likelihood of host survival to such an extreme extent, and will confer only minor changes in host fitness. Due to the large population sizes of bacteria and the time scales involved, the process and outcome of HGT are often not amenable to experimental investigation. Population genetic modeling of the growth dynamics of bacteria with differing HGT rates and resulting fitness changes is therefore necessary to guide sampling design and predict realistic time frames for detection of HGT, as it occurs in laboratory or natural settings. Here we review the key population genetic parameters, consider their complexity and highlight knowledge gaps for further research.

Outcome of the European Member States and Public consultations on the draft guidance for the risk assessment of the presence at low level of genetically modified plant material in imported food and feed under Regulation (EC) No 1829/2003

“…real time PCR) this single recombinant would be only detectable if 3 tons of soil would have been sampled (please see table 1 in reference Heinemann and Traavik 2004). Horizontal gene transfer under field conditions is hard to detect: But not because this process is not taking place but because the available tools for analysing this process are inadequate (Nielsen et al 2014). Additionally, we would also like to refer to several reports indicating plant-to-bacteria gene transfer in natural environments (Netherwood et al 2004;Pontiroli et al 2009;Pontiroli et al 2010;Nikolaidis et al 2014).…”

Critical mutation rate in a population with horizontal gene transfer

“…In silico evolution enables each parameter to be tested independently or in combination as a means of understanding the un-derlying mechanisms of evolution dependent on parameters such as population size, generation time, HGT frequency, and change in relative fitness of recipient cells (Hindré et al, 2012). For example, modelling has facilitated prediction of HGT detectability in bacterial populations growing both in vitro and in vivo (Nielsen et al, 2014).…”

“…It was first identified in 1928 when it was noted that virulence could be passed horizontally from virulent to non-virulent strains of Streptococcus pneumoniae via transformation (Griffith, 1928;Ravenhall et al, 2015). HGT has also been shown to occur via transduction and conjugation (Tatum and Lederberg, 1947;Zinder and Lederberg, 1952;Jones and Sneath, 1970), increasing genetic diversity in bacteria above the level that would be accessible via mutation alone (Nielsen et al, 2014). The majority of HGT events lead only to minimal changes in recipient fitness, an exception being antibiotic resistance; the presence of antibiotics leads to strong positive selection for resistance genes (Nielsen et al, 2014).…”

“…HGT has also been shown to occur via transduction and conjugation (Tatum and Lederberg, 1947;Zinder and Lederberg, 1952;Jones and Sneath, 1970), increasing genetic diversity in bacteria above the level that would be accessible via mutation alone (Nielsen et al, 2014). The majority of HGT events lead only to minimal changes in recipient fitness, an exception being antibiotic resistance; the presence of antibiotics leads to strong positive selection for resistance genes (Nielsen et al, 2014). Advances in whole genome sequencing have enabled the amount of genetic material acquired via HGT to be quantified; Ochman et al (2000) review a distribution of estimates of between 0 and 12.8% of the genome designated as horizontally acquired in a variety of species, while Cooper (2007) gives an estimate of 1 × 10 −4 genes transferred horizontally per cell per generation in Escherichia coli.…”

Explanatory note on DNA sequence similarity searches in the context of the assessment of horizontal gene transfer from plants to microorganisms

“…Should such transfer occur, it is considered to be several orders of magnitude lower than between bacteria. In the environment, HGT is strongly limited by physical and biological barriers inherent in the transfer process itself (Nielsen et al, 1998(Nielsen et al, , 2014Thomas and Nielsen, 2005;EFSA, 2009). …”