Diverse Horizontally-Acquired Gene Clusters Confer Sucrose Utilization to Different Lineages of the Marine Pathogen Photobacterium damselae subsp. damselae

Abstract

The ability to metabolize sucrose is a variable trait within the family Vibrionaceae. The marine bacterium Photobacterium damselae subsp. damselae (Pdd), pathogenic for marine animals and humans, is generally described as negative for sucrose utilization (Scr−). Previous studies have reported sucrose-utilizing isolates (Scr+), but the genetic basis of this variable phenotype remains uncharacterized. Here, we carried out the genome sequencing of five Scr+ and two Scr− Pdd isolates and conducted a comparative genomics analysis with sixteen additional Pdd genomes sequenced in previous studies. We identified two different versions of a four-gene cluster (scr cluster) exclusive of Scr+ isolates encoding a PTS system sucrose-specific IIBC component (scrA), a fructokinase (scrK), a sucrose-6-phosphate hydrolase (scrB), and a sucrose operon repressor (scrR). A scrA deletion mutant did not ferment sucrose and was impaired for growth with sucrose as carbon source. Comparative genomics analyses suggested that scr clusters were acquired by horizontal transfer by different lineages of Pdd and were inserted into a recombination hot-spot in the Pdd genome. The incongruence of phylogenies based on housekeeping genes and on scr genes revealed that phylogenetically diverse gene clusters for sucrose utilization have undergone extensive horizontal transfer among species of Vibrio and Photobacterium.

Identification of a chromosomally-encoded sucrose operon-like gene cluster in Vibrio parahaemolyticus strain PH05 isolated from Negros Island, Philippines

“…The ability to metabolize sucrose is a variable trait in the family Vibrionaceae, and this has been the basis of isolation using the Thiosulfate-citrate-bile salts-sucrose (TCBS) agar [1]. TCBS is a selective and differential culture medium used in the selective isolation and cultivation of Vibrio species [36, 56].…”

The Acquisition of the scr Gene Cluster Encoding Sucrose Metabolization Enzymes Enables Strains of Vibrio parahaemolyticus and Vibrio vulnificus to Utilize Sucrose as Carbon Source

“…The arrangement of scr genes in Photobacterium damselae, a marine species belonging to the family Vibrionaceae, is also very similar to that of V. alginolyticus and V. parahaemolyticus (Abushattal et al, 2020). The authors performed a bioinformatic analysis for scr genes in several published genomes of Vibrio and Photobacterium species which revealed the arrangement of scrA, scrK, and scrB with the putative regulator gene scrR upstream of scrA in many species of these two genera (Abushattal et al, 2020).…”

“…In Photobacterium damselae two direct repeat sequences flanking the four scr genes were identified and it was hypothesized that these sequences may be involved in horizontal gene transfer ( Abushattal et al, 2020 ). We could not find repeat sequences flanking the scr genomic cluster in our V. parahaemolyticus genomes.…”

“…Upstream of scrA a gene encoding a regulator ( scrR ) is found whose transcription is in the opposite direction to scrA, scrK , and scrB . In one recent paper the genetics of sucrose metabolism in several Vibrio and Photobacterium species was addressed ( Abushattal et al, 2020 ) and in a second paper the genes of a sucrose-positive V. parahaemolyticus isolate were identified ( De Mesa et al, 2021 ). The arrangement of sucrose utilization genes of most species correspond to that of V. alginolyticus .…”

Pathogenicity potential of antimicrobial‐resistant Photobacterium damselae subsp. damselae isolated from maricultured and wild‐caught fish of the southeast coast of India

“…P. damselae subsp. damselae grown on TCBS produces green colonies and occasionally yellow colonies (Abushattal et al, 2020). Those green colonies were selected randomly and streaked onto trypticase soya agar (TSA) slants with 2% NaCl and incubated at 27°C for 24 h. Pure presumptive colonies cultures were stored at −80°C in trypticase soya broth with 15% (v/v) glycerol until use (Fouz et al, 2000).…”