The Pathogen of the Great Barrier Reef Sponge Rhopaloeides odorabile Is a New Strain of Pseudoalteromonas agarivorans Containing Abundant and Diverse Virulence-Related Genes

Abstract

Sponge diseases have increased dramatically, yet the causative agents of disease outbreaks have eluded identification. We undertook a polyphasic taxonomic analysis of the only confirmed sponge pathogen and identified it as a novel strain of Pseudoalteromonas agarivorans. 16S ribosomal RNA (rRNA) and gyraseB (gyrB) gene sequences along with phenotypic characteristics demonstrated that strain NW4327 was most closely related to P. agarivorans. DNA-DNA hybridization and in silico genome comparisons established NW4327 as a novel strain of P. agarivorans. Genes associated with type IV pili, mannose-sensitive hemagglutinin pili, and curli formation were identified in NW4327. One gene cluster encoding ATP-binding cassette (ABC) transporter, HlyD and TolC, and two clusters related to the general secretion pathway indicated the presence of type I secretion system (T1SS) and type II secretion system (T2SS), respectively. A contiguous gene cluster of at least 19 genes related to type VI secretion system (T6SS) which included all 13 core genes was found. The absence of T1SS and T6SS in nonpathogenic P. agarivorans S816 established NW4327 as the virulent strain. Serine proteases and metalloproteases of the classes S8, S9, M4, M6, M48, and U32 were identified in NW4327, many of which can degrade collagen. Collagenase activity in NW4327 and its absence in the nonpathogenic P. agarivorans KMM 255(T) reinforced the invasiveness of NW4327. This is the first report unambiguously identifying a sponge pathogen and providing the first insights into the virulence genes present in any pathogenic Pseudoalteromonas genome. The investigation supports a theoretical study predicting high abundance of terrestrial virulence gene homologues in marine bacteria.

New Genomic Insights into “Entotheonella” Symbionts in Theonella swinhoei: Mixotrophy, Anaerobic Adaptation, Resilience, and Interaction

“…Some extracellular proteolytic enzymes, mainly of the metalloprotease group, have been found to be virulence factors (Costa et al, 2015). Only one secreted collagenase (EC 3.4.24.3) was found in “ Entotheonella ,” whereas the known sponge pathogen Pseudoalteromonas agarivorans NW4327 contained 30 secreted serine proteases and metalloproteases (Choudhury et al, 2015). Here we hypothesize that the ability to degrade collagen might be essential for “ Entotheonella ” to obtain space in the sponge mesohyl.…”

“…All the core components of T6SSs (Boyer et al, 2009) were detected in “ Candidatus Entotheonella gemina ” (TSY2 and v4.2), whereas the spike protein VgrG was missing in “ Candidatus Entotheonella factor ” (TSY1 and v4.3). A previous study of the sponge pathogen P. agarivorans NW4327 revealed the existence of 19 genes related to T6SSs (Choudhury et al, 2015). This study is the second report of T6SSs in a sponge symbiont.…”

Antimicrobial Potential of Bacteria Associated with Marine Sea Slugs from North Sulawesi, Indonesia

“…The bacteria are frequently associated with macroorganisms and therefrom it can be expected that the chemical molecules fulfill an important role as signaling and/or defense molecules. These bacteria are mostly associated with healthy animals and plants, only few reports exist that these strains act opportunistic or pathogenic (Choudhury et al, 2015). Therefore, a positive effect on the implementation of the microbiome for the macroorganism can be expected, making them a key partner in marine holobionts.…”

Brown Rot Syndrome and Changes in the Bacterial Сommunity of the Baikal Sponge Lubomirskia baicalensis

“…Some detailed investigations revealed several putative pathogens within this order. Species of the Hormoscilla genus were involved in mangrove sponge disease (MSD) [48] and detected in necrosis of Callyspongia (Euplacella) aff. biru [40].…”

“…Several studies have hypothesized on the putative role of viruses, fungi, cyanobacteria, Alphaproteobacteria, Gammaproteobacteria, Epsilonproteobacteria, Firmicutes, and Bacteroidetes [16,19,34,[40][41][42][43][44][45][46][47]. However, there is only one case in which the fulfillment of Koch's Postulate has enabled the identification of a new Alphaproteobacteria, Pseudoalteromonas agarivorans, as the pathogen behind the disease of Rhopaloeides odorabile [38,48].…”