Aquatic adaptation of a laterally acquired pectin degradation pathway in marine gammaproteobacteria

Abstract

Summary Mobile genomic islands distribute functional traits between microbes and habitats, yet it remains unclear how their proteins adapt to new environments. Here we used a comparative phylogenomic and proteomic approach to show that the marine bacterium Pseudoalteromonas haloplanktis ANT/505 acquired a genomic island with a functional pathway for pectin catabolism. Bioinformatics and biochemical experiments revealed that this pathway encodes a series of carbohydrate‐active enzymes including two multi‐modular pectate lyases, PelA and PelB. PelA is a large enzyme with a polysaccharide lyase family 1 (PL1) domain and a carbohydrate esterase family 8 domain, and PelB contains a PL1 domain and two carbohydrate‐binding domains of family 13. Comparative phylogenomic analyses indicate that the pathway was most likely acquired from terrestrial microbes, yet we observed multi‐modular orthologues only in marine bacteria. Proteomic experiments showed that P. haloplanktis ANT/505 secretes both pectate lyases into the environment in the presence of pectin. These multi‐modular enzymes may therefore represent a marine innovation that enhances physical interaction with pectins to reduce loss of substrate and enzymes by diffusion. Our results revealed that marine bacteria can catabolize pectin, and highlight enzyme fusion as a potential adaptation that may facilitate microbial consumption of polymeric substrates in aquatic environments.

Biphasic cellular adaptations and ecological implications of Alteromonas macleodii degrading a mixture of algal polysaccharides

“…The environmental importance of alginate is reflected by the occurrence of alginate lyases in various bacterial taxa [48]. Pectin, largely composed of α-(1-4)-galacturonate, is abundant in terrestrial plants, but the presence of complex pectinolytic operons in marine bacteria [49] and up to 0.3 µM galacturonate during phytoplankton blooms [50] suggest that pectinous substrates are common in marine systems as well. Due to their gelling capacities, alginate and pectin may also occur in transparent exopolymer particles [50,51].…”

100 Days of marine Synechococcus–Ruegeria pomeroyi interaction: A detailed analysis of the exoproteome

“…For example, the most abundant enzyme detected, i.e., the pectate lyase-like protein, was annotated as a hypothetical protein and only suggested here as a hydrolytic enzyme for polysaccharides based on a pectate lyase-like domain it contains. Other pectate lyases have been detected in marine microbes, but these seem to have been acquired from a terrestrial origin (Hehemann et al, 2017). Nevertheless, this is not the norm and most marine microbes have a novel array of untapped hydrolytic enzymes that largely differ from their well-known terrestrial counterparts (Hehemann et al, 2014), which require further characterization.…”

Dissemination and loss of a biofilm‐related genomic island in marine Pseudoalteromonas mediated by integrative and conjugative elements

“…; Hehemann et al . ). The mechanism used to transfer GIs devoid of recombination and conjugation modules remains largely unexplored.…”

“…Marine Gammaproteobacteria, including Pseudoalteromonas, Alteromonas, Shewanella and Vibrio, are the genera that most commonly adopt a particle-associated lifestyle in marine environments (Garcia-Martinez et al, 2002;Mai-Prochnow et al, 2006;Mahmoud, 2015). Comparative genomics has shown that these species often contain similar mobile genetic elements and that many of these species cohabit in the same microniches, e.g., marine biofilms (Daccord et al, 2013;Hehemann et al, 2017). The spread of mobile genetic elements by horizontal gene transfer is more frequent in biofilms than in free-living bacteria (Hausner and Wuertz, 1999;Sorensen et al, 2005).…”

“…A recent study demonstrated that two GIs with integrases and one ICE without an integrase in Mesorhizobium ciceri can be assembled into a tripartite ICE and co-transfer (Haskett et al, 2016). However, many GIs that harbour conserved cargo genes but do not carry elements for recombination or transfer are also found in distantly related strains (Daccord et al 2013;Hehemann et al 2017). The mechanism used to transfer GIs devoid of recombination and conjugation modules remains largely unexplored.…”