Abstract
BackgroundBacteria play critical roles in marine nutrient cycles by incorporating and redistributing dissolved organic matter (DOM) and inorganic nutrients in the ocean. TonB-dependent transporter (TBDT) proteins allow Gram-negative bacteria to take up scarce resources from nutrient-limiting environments as well as siderophores, heme, vitamin B12, and recently identified carbohydrates. Thus, the characterization of TBDT distribution and functions is essential to better understand the contribution TBDT to DOM assimilation and its consequences on nutrient cycling in the environment.Methodology/Principal FindingsThis study presents the distribution of encoded known and putative TBDT proteins in the genomes of microorganisms and from the Global Ocean Survey data. Using a Lek clustering algorithm and substrate specificities, the TBDT sequences were mainly classified into the following three groups: (1) DOM transporters; (2) Siderophores/Vitamins transporters; and (3) Heme/Hemophores/Iron(heme)-binding protein transporters. Diverse TBDTs were found in the genomes of oligotroph Citromicrobium bathyomarinum JL354 and Citromicrobium sp JLT1363 and were highly expressed in the stationary phase of bacterial growth. The results show that the Gammaproteobacteria and the Cytophaga-Flavobacterium-Bacteroides (CFB) group bacteria accounted for the majority of the TBDT gene pool in marine surface waters.Conclusions/SignificanceThe results of this study confirm the ecological importance of TBDTs in DOM assimilation for bacteria in marine environments owing to a wide range of substrate utilization potential in the ubiquitous Gammaproteobacteria and CFB group bacteria.
Highlights
Bacteria play important roles in ocean carbon and nutrient cycling by incorporating and redistributing dissolved organic matter (DOM) and inorganic nutrients [1], [2]
This study primarily focuses on TonB-dependent transporter (TBDT) in marine bacteria, and species were included such that all the major groups of bacteria are covered
The results of the analysis of the genetic contexts near the TBDT show that some TBDT genes were closely associated with the carbohydrate, amino acid, or other substrate metabolism enzymes in the operons (Figures 4 and 5), suggesting that these genes are functionally linked and may play important roles in diverse DOM uptake for marine bacteria, but are not limited to iron and vitamin B12 uptake only
Summary
Bacteria play important roles in ocean carbon and nutrient cycling by incorporating and redistributing dissolved organic matter (DOM) and inorganic nutrients [1], [2]. ABC transporters are ubiquitous in bacteria and function in the import of growth substrates or factors, including carbohydrates, amino acids, polypeptides, vitamins, and metal-chelate complexes [9]. Sphingomonas wittichii RW1 affiliated with Sphingomonadales currently contains the most TBDTs among all microorganisms [25] These TBDTs are used by bacteria for uptake of diverse substrates, including aromatic compounds [25]. Bacteria play critical roles in marine nutrient cycles by incorporating and redistributing dissolved organic matter (DOM) and inorganic nutrients in the ocean. TonB-dependent transporter (TBDT) proteins allow Gram-negative bacteria to take up scarce resources from nutrient-limiting environments as well as siderophores, heme, vitamin B12, and recently identified carbohydrates. The characterization of TBDT distribution and functions is essential to better understand the contribution TBDT to DOM assimilation and its consequences on nutrient cycling in the environment
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