Hydrophobic organic compounds (mainly lipids and hydrocarbons) represent a significant part of the organic matter in marine waters, and their degradation has an important impact in the carbon fluxes within oceans. However, because they are nearly insoluble in the water phase, their degradation by microorganisms occurs at the interface with water and thus requires specific adaptations such as biofilm formation. We show that Marinobacter hydrocarbonoclasticus SP17 develops biofilms, referred to as oleolytic biofilms, on a large variety of hydrophobic substrates, including hydrocarbons, fatty alcohols, fatty acids, triglycerides, and wax esters. Microarray analysis revealed that biofilm growth on n-hexadecane or triolein involved distinct genetic responses, together with a core of common genes that might concern general mechanisms of biofilm formation. Biofilm growth on triolein modulated the expression of hundreds of genes in comparison with n-hexadecane. The processes related to primary metabolism and genetic information processing were downregulated. Most of the genes that were overexpressed on triolein had unknown functions. Surprisingly, their genome localization was restricted to a few regions identified as putative genomic islands or mobile elements. These results are discussed with regard to the adaptive responses triggered by M. hydrocarbonoclasticus SP17 to occupy a specific niche in marine ecosystems.
f Marinobacter hydrocarbonoclasticus SP17 forms biofilms specifically at the interface between water and hydrophobic organic compounds (HOCs) that are used as carbon and energy sources. Biofilm formation at the HOC-water interface has been recognized as a strategy to overcome the low availability of these nearly water-insoluble substrates. Here, we present the genome sequence of SP17, which could provide further insights into the mechanisms of enhancement of HOCs assimilation through biofilm formation.H ydrophobic organic compounds (HOCs) encompassing lipids, hydrocarbons, and some organic pollutants are widely distributed in the environment but are weakly soluble in water and as a consequence poorly available for assimilation by heterotrophic bacteria. Biofilm formation at the HOC-water interface is a strategy employed by Marinobacter hydrocarbonoclasticus SP17 (ATCC 49840) to overcome the low bioavailability of HOCs. SP17 was isolated from chronically oil-contaminated sediment for its ability to use alkanes as the sole carbon and energy source (5). M. hydrocarbonoclasticus is a Gram-negative, aerobic, motile, nonspore-forming, and rod-shaped bacterium (5). It exhibits extreme halotolerance (0.08 to 3.5 M NaCl) and synthesizes ectoine as an osmoprotectant (2, 3).SP17 adheres and forms biofilms on alkanes and produces an extracellular-surface-active compound (2, 6). Physiological and proteomic studies revealed that biofilm formation is an efficient strategy to colonize hydrophobic interfaces (1,11,12). SP17 forms biofilms at the interface between aqueous-phase and HOC substrates like n-alkanes, fatty alcohols, or apolar lipids, such as wax esters and triacylglycerols. In contrast, biofilms were not observed on the nonmetabolizable compounds (n-C 32 alkanes, pristane, and heptamethylnonane) and glass or plastics (7). The discrimination between metabolizable and nonmetabolizable compounds indicates that at some level, biofilm formation is controlled by the presence of a nutritive interface. Adhesion and biofilm formation could be a behavioral strategy to acquire carbon and energy from HOCs contained in marine aggregates.The sequencing of the M. hydrocarbonoclasticus SP17 genome was obtained using a conventional whole-genome shotgun strategy with three libraries (3-, 10-, and 25-kb fragments) on ABI3730 sequencers. Assembly was done using the Phred/Phrap/Consed software package (www.phrap.org) with primer walking, PCR, and in vitro transposition technology (Template generation system II kit; Finnzyme, Espoo, Finland) as finishing steps, yielding a single contig molecule without gaps. Automatic genome annotation was performed using the MAGE annotation server (9, 10) followed by manual annotation. The genome of SP17 encompasses a unique chromosome with a similar GϩC content (57.43%) to but a smaller size (3989,480 bases) than that of the other Marinobacter genomes (ranging between 4,333 and 4,894 kb) (4, 8, 13). The SP17 genome contains 3 rRNA operons, 50 tRNA genes, and 3807 protein-coding sequences (CDSs) (967.89-b...
Many hydrocarbon degrading bacteria form biofilms at the hydrocarbon-water interface to overcome the low accessibility of these poorly water-soluble substrates. In order to gain insight into the cellular functions involved, we undertook a proteomic analysis of Marinobacter hydrocarbonoclasticus SP17 biofilm developing at the hexadecane-water interface. Biofilm formation on hexadecane led to a global change of the cell physiology involving modulation of the expression of 573 out of 1144 detected proteins when compared with planktonic cells growing on acetate. Biofilm cells overproduced a protein, encoded by MARHY0478 that contains a conserved domain belonging to the family of the outer membrane transporters of hydrophobic compounds. Homologs of MARHY0478 were exclusively found in marine bacteria degrading alkanes or possessing alkane degradation genes and hence presumably constitute a family of alkane transporter specific to marine bacteria. Interestingly, we also found that sessile cells growing on hexadecane overexpressed type VI secretion system components. This secretion system has been identified as a key factor in virulence and in symbiotic interaction with host organisms. This observation is the first experimental evidence of the contribution of a type VI secretion system to environmental adaptation and raises the intriguing question about the role of this secretion machine in alkane assimilation.
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