Costs and benefits of natural transformation in Acinetobacter baylyi

Hülter, Nils; Sørum, Vidar; Borch-Pedersen, Kristina; Liljegren, Mikkel Meyn; Utnes, Ane; Primicerio, Raul; Harms, Klaus; Johnsen, Pål Jarle

doi:10.1186/s12866-017-0953-2

Cited by 22 publications

(30 citation statements)

References 74 publications

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“…Based on our observation that pRL153-GFP could be efficiently activated for conjugation, we developed a mobilizable derivate of the previously described ColE-derived gene targeting plasmid vector pGT41 ( Kickstein et al, 2007 ; Overballe-Petersen et al, 2013 ; Hülter et al, 2017 ) that can be used for the generation of chromosomal deletion mutations in Curvibacter (see Supplementary File 1 for details).…”

Section: Resultsmentioning

confidence: 99%

Carrying Capacity and Colonization Dynamics of Curvibacter in the Hydra Host Habitat

et al. 2018

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Most eukaryotic species are colonized by a microbial community – the microbiota – that is acquired during early life stages and is critical to host development and health. Much research has focused on the microbiota biodiversity during the host life, however, empirical data on the basic ecological principles that govern microbiota assembly is lacking. Here we quantify the contribution of colonizer order, arrival time and colonization history to microbiota assembly on a host. We established the freshwater polyp Hydra vulgaris and its dominant colonizer Curvibacter as a model system that enables the visualization and quantification of colonizer population size at the single cell resolution, in vivo, in real time. We estimate the carrying capacity of a single Hydra polyp as 2 × 105 Curvibacter cells, which is robust among individuals and time. Colonization experiments reveal a clear priority effect of first colonizers that depends on arrival time and colonization history. First arriving colonizers achieve a numerical advantage over secondary colonizers within a short time lag of 24 h. Furthermore, colonizers primed for the Hydra habitat achieve a numerical advantage in the absence of a time lag. These results follow the theoretical expectations for any bacterial habitat with a finite carrying capacity. Thus, Hydra colonization and succession processes are largely determined by the habitat occupancy over time and Curvibacter colonization history. Our experiments provide empirical data on the basic steps of host-associated microbiota establishment – the colonization stage. The presented approach supplies a framework for studying habitat characteristics and colonization dynamics within the host–microbe setting.

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Section: Resultsmentioning

confidence: 99%

Carrying Capacity and Colonization Dynamics of Curvibacter in the Hydra Host Habitat

et al. 2018

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“…Results demonstrated negligible changes in transformation frequencies with both methods (Figure 3 ), which indicates that natural transformation is stable within a short-term passage in this species. This also suggests that natural transformability varies greatly in different species due to different competence regulatory elements/circuits and/or environmental cues of triggering competence (Krüger and Stingl, 2011 ; Seitz and Blokesch, 2013 ; Hülter et al, 2017 ).…”

Section: Resultsmentioning

confidence: 99%

Basic Characterization of Natural Transformation in a Highly Transformable Haemophilus parasuis Strain SC1401

Dai

Chang

et al. 2018

Front. Cell. Infect. Microbiol.

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Haemophilus parasuis causes Glässer's disease and pneumonia, incurring serious economic losses in the porcine industry. In this study, natural competence was investigated in H. parasuis. We found competence genes in H. parasuis homologous to ones in Haemophilus influenzae and a high consensus battery of Sxy-dependent cyclic AMP (cAMP) receptor protein (CRP-S) regulons using bioinformatics. High rates of natural competence were found from the onset of stationary-phase growth condition to mid-stationary phase (OD600 from 0.29 to 1.735); this rapidly dropped off as cells reached mid-stationary phase (OD600 from 1.735 to 1.625). As a whole, bacteria cultured in liquid media were observed to have lower competence levels than those grown on solid media plates. We also revealed that natural transformation in this species is stable after 200 passages and is largely dependent on DNA concentration. Transformation competition experiments showed that heterogeneous DNA cannot outcompete intraspecific natural transformation, suggesting an endogenous uptake sequence or other molecular markers may be important in differentiating heterogeneous DNA. We performed qRT-PCR targeting multiple putative competence genes in an effort to compare bacteria pre-cultured in TSB++ vs. TSA++ and SC1401 vs. SH0165 to determine expression profiles of the homologs of competence-genes in H. influenzae. Taken together, this study is the first to investigate natural transformation in H. parasuis based on a highly naturally transformable strain SC1401.

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“…The results obtained are robust, even if we consider the inherent risks associated with transformation: the possibility of acquiring toxic and highly detrimental genes and the recombination intermediates that can jeopardize chromosome integrity 39,40 . To account for such a transformation cost, we implemented a probability of cell lysis during transformation events.…”

Section: Transformable Cells Are Competitive In Stochastic Environmentsmentioning

confidence: 76%

Bacterial transformation buffers environmental fluctuations through the reversible integration of mobile genetic elements

Carvalho

Fouchet

Danesh

et al. 2019

Preprint

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Horizontal gene transfer (HGT) is known to promote the spread of genes in bacterial communities, which is of primary importance to human health when these genes provide resistance to antibiotics. Among the main HGT mechanisms, natural transformation stands out as being widespread and encoded by the bacterial core genome. From an evolutionary perspective, transformation is often viewed as a mean to generate genetic diversity and mixing within bacterial populations. However, another recent paradigm proposes that its main evolutionary function would be to cure bacterial genomes from their parasitic mobile genetic elements (MGEs). Here, we propose to combine these two seemingly opposing points of view because MGEs, although costly for bacterial cells, can carry functions that are point-in-time beneficial to bacteria under stressful conditions (e.g. antibiotic resistance genes under antibiotic exposure). Using computational modeling, we show that, in stochastic environments (unpredictable stress exposure), an intermediate transformation rate maximizes bacterial fitness by allowing the reversible integration of MGEs carrying resistance genes but costly for the replication of host cells. By ensuring such reversible genetic diversification (acquisition then removal of MGEs), transformation would be a key mechanism for stabilizing the bacterial genome in the long term, which would explain its striking conservation.

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Costs and benefits of natural transformation in Acinetobacter baylyi

Cited by 22 publications

References 74 publications

Carrying Capacity and Colonization Dynamics of Curvibacter in the Hydra Host Habitat

Carrying Capacity and Colonization Dynamics of Curvibacter in the Hydra Host Habitat

Basic Characterization of Natural Transformation in a Highly Transformable Haemophilus parasuis Strain SC1401

Bacterial transformation buffers environmental fluctuations through the reversible integration of mobile genetic elements

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