Comparative genome analysis of marine purple sulfur bacterium Marichromatium gracile YL28 reveals the diverse nitrogen cycle mechanisms and habitat-specific traits

Abstract

Mangrove ecosystems are characteristic of the high salinity, limited nutrients and S-richness. Marichromatium gracile YL28 (YL28) isolated from mangrove tolerates the high concentrations of nitrite and sulfur compounds and efficiently eliminates them. However, the molecular mechanisms of nitrite and sulfur compounds utilization and the habitat adaptation remain unclear in YL28. We sequenced YL28 genome and further performed the comparative genome analysis in 36 purple bacteria including purple sulfur bacteria (PSB) and purple non-sulfur bacteria (PNSB). YL28 has 6 nitrogen cycle pathways (up to 40 genes), and possibly removes nitrite by denitrification, complete assimilation nitrate reduction and fermentative nitrate reduction (DNRA). Comparative genome analysis showed that more nitrogen utilization genes were detected in PNSB than those in PSB. The partial denitrification pathway and complete assimilation nitrate reduction were reported in PSB and DNRA was reported in purple bacteria for the first time. The three sulfur metabolism genes such as oxidation of sulfide, reversed dissimilatory sulfite reduction and sox system allowed to eliminate toxic sulfur compounds in the mangrove ecosystem. Several unique stress response genes facilitate to the tolerance of the high salinity environment. The CRISPR systems and the transposon components in genomic islands (GIs) likely contribute to the genome plasticity in purple bacteria.

Figure 1

Phylogenetic analyses between PSB and PNSB. The NJ algorithm tree of 16S rRNA genes of 36 strains from purple bacteria by the MEGA 6.06 (A); the Mauve guide tree of the 35 strains based on whole-genomic similarity at the nucleotide level through multiple genome comparison tool Mauve (B); the NJ tree of 77 conserved proteins shared among the 36 strains by the BPGA (C).

Figure 2

Pan, core and singleton genome evolution according to the number of selected purple bacteria genomes. (A) Number of genes (core genome and Pan-genome) for the selected purple bacteria genomes sequentially added. (B) Number of unique genes for the selected purple bacteria genomes sequentially added.

Figure 3

The model of nitrogen metabolism in M. gracile YL28. There are six nitrogen metabolic pathways in YL28 whose key enzyme confirmed by CDART and CDD. (A) Ammonification pathway; (B) ammonium assimilation pathway; (C) fermentative nitrate reduction; (D) denitrification; (E) assimilation nitrate reduction; (F) nitrogen fixation.

Figure 4

Whole-genome comparisons in three genera of purple bacteria. The color intensity in each ring represents the BLAST match identity. (A) Whole-genome comparison of all the strains considered in this work; (B) Whole-genome comparisons of strains of purple sulfur bacteria and T118, IL144. The color intensity in each ring represents the BLAST match identity. from inner to outer ring: M. purpuratum 984, A. vinosum DSM 180, T. violascens DSM 198, T. mobilis 8321, Ectothiorhodospira sp. BSL-9, H. halophila SL1, R. gelatinosus IL144, R. ferrireducens T118. (C) Whole-genome comparisons of 12 strains of purple non-sulfur bacteria. The color intensity in each ring represents the BLAST match identity. from inner to outer ring: R. palustris BisA53, BisB18, BisB5, DX-1, HaA2, TIE-1, B. viridis, B. viridis ATCC19567, B. viridis DSM133, Rhodoplanes sp. Z2-YC6860, R. vannielii ATCC 17100. (D) Whole-genome comparisons 11 strains of two gena in Rhodobacter and Rhodovulum in purple non-sulfur bacteria. The color intensity in each ring represents the BLAST match identity from inner to outer ring: R. capsulatus SB 1003, Rhodobacter sp. LPB0142, R. sphaeroides ATCC 17025, R. sphaeroides ATCC 17029, R. sphaeroides KD131, R. sphaeroides MBTLJ-13, R. sphaeroides MBTLJ-8, R. sulfidophilum DSM1374, R. sulfidophilum DSM2351, R. sulfidophilum SNK001; (E) whole-genome comparisons in Rhodobacter, from inner to outer ring: R. rubrum F11, R. centenum SW, P. photometricum DSM 122.