Research Article: Comparative genome analysis reveals niche-specific genome expansion in Acinetobacter baumannii strains

Date Published: June 13, 2019

Publisher: Public Library of Science

Author(s): Harshita Yakkala, Devyani Samantarrai, Michael Gribskov, Dayananda Siddavattam, Feng Gao.

http://doi.org/10.1371/journal.pone.0218204

Abstract

The nosocomial pathogen Acinetobacter baumannii acquired clinical significance due to the rapid development of its multi-drug resistant (MDR) phenotype. A. baumannii strains have the ability to colonize several ecological niches including soil, water, and animals, including humans. They also survive under extremely harsh environmental conditions thriving on rare and recalcitrant carbon compounds. However, the molecular basis behind such extreme adaptability of A. baumannii is unknown. We have therefore determined the complete genome sequence of A. baumannii DS002, which was isolated from agricultural soils, and compared it with 78 complete genome sequences of A. baumannii strains having complete information on the source of their isolation. Interestingly, the genome of A. baumannii DS002 showed high similarity to the genome of A. baumannii SDF isolated from the body louse. The environmental and clinical strains, which do not share a monophyletic origin, showed the existence of a strain-specific unique gene pool that supports niche-specific survival. The strains isolated from infected samples contained a genetic repertoire with a unique gene pool coding for iron acquisition machinery, particularly those required for the biosynthesis of acinetobactin. Interestingly, these strains also contained genes required for biofilm formation. However, such gene sets were either partially or completely missing in the environmental isolates, which instead harbored genes required for alternate carbon catabolism and a TonB-dependent transport system involved in the acquisition of iron via siderophores or xenosiderophores.

Partial Text

A surge in the number of multi-drug resistant (MDR) bacteria has increased the severity of many bacterial diseases. The number of infections caused by the MDR strains has almost quadrupled in the last two decades [1, 2]. Of these, the ESKAPE pathogens comprising of Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter species form the major proportion of MDR and extremely drug resistance (XDR) strains [3, 4]. The genus Acinetobacter are Gram-negative bacteria belonging to the class Gammaproteobacteria. Nearly 55 different species of Acinetobacter have been isolated from sources as varied as water [5], soil [6], hospitals [7, 8], body fluids [9, 10], and even body lice [11]. Almost all are known to cause human diseases. Acinetobacter baumannii is the predominant species of the genus and accounts for about 80% of reported Acinetobacter infections (https://www.cdc.gov/hai/organisms/acinetobacter.html), which range from pneumonia to serious blood or wound infections, soft tissue infections, and secondary meningitis [12–14]. The symptoms vary depending on the severity of the infection, but strains can also be asymptomatic, residing in tracheostomy sites or open wounds. A. baumannii strains are known for their genome plasticity and the ability to survive on abiotic surfaces [15, 16]. They acquire genes through conventional horizontal gene transfer (HGT), as well as through membrane vesicles [17–22]. Such robust gene acquisition contributes to the evolution of A. baumannii strains exhibiting MDR and XDR.

Isolation of MDR strains of A. baumannii has gradually increased ever since they were first identified during an outbreak at a hospital in New York City [88]. In the 1970s, most of the strains were sensitive to well-known antibiotics. Meanwhile, during the span of forty years nearly 70% of the clinical isolates have acquired MDR status [2]. Carbapenems, once considered to be the linchpin against MDR A. baumannii strains were found to be ineffective in controlling MDR strains of A. baumannii. Such a rapid increase in drug resistance requires deeper insights into the correlation between the evolution of A. baumannii and their adaptation to a pathogenic lifestyle.

The comparative genome analysis highlighted the selective expansion of unique, niche-specific genome content in A. baumannii. The expanded unique genome content contribute to the strain’s adaptability to different ecological habitats. Our study clearly revealed the expansion of drug-resistance genes only in clinical isolates, as it confers a selective advantage for the survival of clinical isolates in an ecological niche that is frequently exposed to all kinds of antibiotics. Interestingly, no difference in the virolome of the different A. baumannii strains exists. However, the genetic makeup required for biofilm formation, an essential feature for colonization of a host, is only seen in clinical isolates. Because biofilm formation is not essential for the survival of soil isolates, the loss of critical genes involved in biofilm formation is frequently observed. Niche-specific genome expansion has also revealed an impact on carbon metabolism. The pheA found in unique genome content enables the survival of cells using phenol as the sole source of carbon, is only seen in strains that are frequently exposed to phenolic substances.

 

Source:

http://doi.org/10.1371/journal.pone.0218204

 

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