Genomes and Virulence Factors of Novel Bacterial Pathogens Causing Bleaching Disease in the Marine Red Alga Delisea pulchra

Neil Fernandes,Torsten Thomas,Mohammad R Seyedsayamdost,Rebecca J Case,Sharon R Longford,Staffan Kjelleberg,Peter D Steinberg,Debashish Bhattacharya

doi:10.1371/journal.pone.0027387

Abstract

Nautella sp. R11, a member of the marine Roseobacter clade, causes a bleaching disease in the temperate-marine red macroalga, Delisea pulchra. To begin to elucidate the molecular mechanisms underpinning the ability of Nautella sp. R11 to colonize, invade and induce bleaching of D. pulchra, we sequenced and analyzed its genome. The genome encodes several factors such as adhesion mechanisms, systems for the transport of algal metabolites, enzymes that confer resistance to oxidative stress, cytolysins, and global regulatory mechanisms that may allow for the switch of Nautella sp. R11 to a pathogenic lifestyle. Many virulence effectors common in phytopathogenic bacteria are also found in the R11 genome, such as the plant hormone indole acetic acid, cellulose fibrils, succinoglycan and nodulation protein L. Comparative genomics with non-pathogenic Roseobacter strains and a newly identified pathogen, Phaeobacter sp. LSS9, revealed a patchy distribution of putative virulence factors in all genomes, but also led to the identification of a quorum sensing (QS) dependent transcriptional regulator that was unique to pathogenic Roseobacter strains. This observation supports the model that a combination of virulence factors and QS-dependent regulatory mechanisms enables indigenous members of the host alga's epiphytic microbial community to switch to a pathogenic lifestyle, especially under environmental conditions when innate host defence mechanisms are compromised.

Highlights

Disease is increasingly viewed as a major factor in marine ecology and its impact is expected to increase with environmental change such as global warming [1,2]
We have recently shown that the bacterial strain R11, which was isolated from D. pulchra, is able to produce in vitro bleaching symptoms that are identical to those observed in the field [7]
Strain R11 has the complete set of biosynthetic pathways for glycolysis, the pentose phosphate pathway and the tricarboxylic acid cycle that are characteristic of heterotrophic bacteria, as well as the pathways required for biosynthesis of nucleotides and all 20 amino acids

Summary

Introduction

Disease is increasingly viewed as a major factor in marine ecology and its impact is expected to increase with environmental change such as global warming [1,2]. D. pulchra can suppress surface colonization by marine microand macro-organisms through the production of brominated furanones [10,11]. These secondary metabolites are potent inhibitors of the N-acyl homoserine lactone (AHL) based quorum sensing (QS) used by some bacteria to coordinate transcription within a population, where the phenotype is beneficial to the population. At elevated temperature (from 19 to 24uC) bacterial cells penetrate through the epidermal layer and invade algal cells without visible cell wall destruction. This process coincides with localized bleaching of the thallus.

Methods

Results

Conclusion