Description of Palleronia rufa sp. nov., a biofilm-forming and AHL-producing Rhodobacteraceae, reclassification of Hwanghaeicola aestuarii as Palleronia aestuarii comb. nov., Maribius pontilimi as Palleronia pontilimi comb. nov., Maribius salinus as Palleronia salina comb. nov., Maribius pelagius as Palleronia pelagia comb. nov. and emended description of the genus Palleronia

Abstract

Strain MOLA 401^T was isolated from marine waters in the southwest lagoon of New Caledonia and was shown previously to produce an unusual diversity of quorum sensing signaling molecules. This strain was Gram-negative, formed non-motile cocci and colonies were caramel. Optimum growth conditions were 30 °C, pH 8 and 3% NaCl (w/v). Based on 16S rRNA gene sequence analysis, this strain was found to be closely related to Pseudomaribius aestuariivivens NBRC 113039^T (96.9% of similarity), Maribius pontilimi DSM 104950^T (96.4% of similarity) and Palleronia marisminoris LMG 22959^T (96.3% of similarity), belonging to the Roseobacter group within the family Rhodobacteraceae. As its closest relatives, strain MOLA 401^T is able to form a biofilm on polystyrene, supporting the view of Roseobacter group strains as prolific surface colonizers. An in-depth genomic study allowed us to affiliate strain MOLA 401^T as a new species of genus Palleronia and to reaffiliate some of its closest relatives in this genus. Consequently, we describe strain MOLA 401^T (DSM 106827^T = CIP 111607^T = BBCC 401^T) for which we propose the name Palleronia rufa sp. nov. We also propose to emend the description of the genus Palleronia and to reclassify Maribius and Hwanghaeicola species as Palleronia species.

Introduction

Most of the Rhodobacteraceae are of marine origin and require sodium ion or combined salt for growth [44], [52]. The family Rhodobacteraceae includes at least 100 genera and among them, the Roseobacter group encompasses more than 70 genera. This family as been proposed by Garrity et al. [21]. It was registered in the validation list no. 107 [32], but was declared illegitimate because it contained the genus Hyphomonas, which was the type of the family Hyphomonadaceae Lee et al. [30]. However, even if Lee et al. modified the classification by placing some species in separate families and the Rhodobacteraceae in the order Caulobacterales, they did not change the family name [30]. Strains belonging to this group share more than 89% identity of 16S rRNA gene sequence [9], [44]. The use of culture-independent approaches provided a basis for recognizing the Roseobacter group as one of the most abundant in marine environments, that represents up to 20% of coastal and 15% of mixed-layer ocean bacterioplankton communities [9], [10]. Wagner-Döbler and Biebl [57] highlighted the importance of this group in cycles of carbon, sulphur and nitrogen in the ocean. The Roseobacter lineage is physiologically heterogeneous. Members of this group exhibit: aerobic anoxygenic photosynthesis, degradation of algal sulphur compounds, carbon monoxide oxidation, degradation of aromatic compounds (e.g. vanillate, benzoate, coumarate), reduction of trace metals, symbiotic and pathogenic relationships, production of bioactive secondary metabolites and quorum sensing (QS), and association with biotic or abiotic surfaces [8], [9], [16], [20], [24], [36], [50], [52], [53]. However, few of these traits are representative of the entire group. The genome plasticity of Roseobacter could explain their wide range of physiological features as well as their wide variety of habitats [9], [57].

QS is used by bacteria to act as coordinated communities. It has been observed to be linked to the production of virulence factors and secondary metabolites, motility, colonization of particulate matter and biofilm formation [5], [6], [15], [22], [37], [51]. QS appears a common trait in the Roseobacter lineage. Homologs of the N-acyl-homoserine lactone (AHL) synthase gene (luxI) were present in more than 80% of roseobacterial genomes available at the time of the study [14], [60]. As AHLs are small secreted diffusing signal molecules implicated in QS in Gram-negative bacteria, this study suggests that a majority of Roseobacter strains possess AHL based QS systems. However, only few characterized Roseobacter isolates have been shown to produce AHL. Roseobacter are often reported as prolific colonizers of inert and living surface in marine environment, and the contribution of QS in these processes is of growing interest.

The present study was undertaken to describe strain MOLA 401^T that was shown to produce a remarkable range of AHLs [18]. The first phylogenetic analyses of strain MOLA 401^T, based on 16S rRNA gene sequence, resulted in its affiliation to the genus Maribius, which belongs to the Roseobacter group in the family Rhodobacteraceae [18]. Three Maribius species have already been described: Maribius salinus, Maribius pelagius and Maribius pontilimi [12], [31]. However, 16S rRNA gene sequences lack the resolution for a proper phylogenetic reconstruction inside the Roseobacter group [9], [33], [52], [59]. Moreover, several strains were described simultaneously, representing a taxonomic challenge to organize this group without redundancy [44]. This is not without consequences, because incorrect species name assignments may cause confusion and mistakes when suggesting evolutionary inference, or in interpreting ecological data concerning this group [33]. We combined classical and genomic markers to define the taxonomic position of strain MOLA 401^T and to clarify that of its closest relatives. In addition, the ability of these bacteria to form biofilms and to produce AHLs, two relevant traits of the Roseobacter group, was demonstrated.