Complete Genome Sequence of <i>Bradyrhizobium</i> sp. S23321: Insights into Symbiosis Evolution in Soil Oligotrophs

Abstract

Bradyrhizobium sp. S23321 is an oligotrophic bacterium isolated from paddy field soil. Although S23321 is phylogenetically close to Bradyrhizobium japonicum USDA110, a legume symbiont, it is unable to induce root nodules in siratro, a legume often used for testing Nod factor-dependent nodulation. The genome of S23321 is a single circular chromosome, 7,231,841 bp in length, with an average GC content of 64.3%. The genome contains 6,898 potential protein-encoding genes, one set of rRNA genes, and 45 tRNA genes. Comparison of the genome structure between S23321 and USDA110 showed strong colinearity; however, the symbiosis islands present in USDA110 were absent in S23321, whose genome lacked a chaperonin gene cluster (groELS3) for symbiosis regulation found in USDA110. A comparison of sequences around the tRNA-Val gene strongly suggested that S23321 contains an ancestral-type genome that precedes the acquisition of a symbiosis island by horizontal gene transfer. Although S23321 contains a nif (nitrogen fixation) gene cluster, the organization, homology, and phylogeny of the genes in this cluster were more similar to those of photosynthetic bradyrhizobia ORS278 and BTAi1 than to those on the symbiosis island of USDA110. In addition, we found genes encoding a complete photosynthetic system, many ABC transporters for amino acids and oligopeptides, two types (polar and lateral) of flagella, multiple respiratory chains, and a system for lignin monomer catabolism in the S23321 genome. These features suggest that S23321 is able to adapt to a wide range of environments, probably including low-nutrient conditions, with multiple survival strategies in soil and rhizosphere.

Nitrogen Fertilization Has a Stronger Effect on Soil Nitrogen-Fixing Bacterial Communities than Elevated Atmospheric CO 2

“…Additionally, the second most common OTU detected in this study (OTU 2 in Table S1) was previously found to be the fourth most frequent OTU 95 in a global survey of nifH sequences (the three OTUs that were observed more frequently were primarily from marine environments) (30). These results confirm the ubiquity of genera such as Azospirillum and Bradyrhizobium, not only as symbiotic N-fixing bacteria, but also potentially as free-living soil diazotrophs (31,32).…”

Non-symbiotic Bradyrhizobium ecotypes dominate North American forest soils

“…Specifically, we were interested in determining whether there are alternative lifestyles that populations within this group occupy besides those associated with the genus. Only one previous study reported the isolation from soil of a Bradyrhizobium strain that lacks the common nod genes (strain S23321; Figure 2), and none have reported strains lacking the nif genes (Okubo et al, 2012). This suggested that OTU1 may be an important component of the nitrogen cycle in these soils.…”

“…Nevertheless, the hypothesized ecological roles of these populations remain focused on symbiosis. Similarly, previous studies have isolated Bradyrhizobium strains diminished or lacking in the ability to fix nitrogen or nodulate leguminous plants from soil, but these strains were described consistently as having transiently abandoned a symbiotic lifestyle or as relics of an ancestral symbiotic genotype (Sachs et al, 2010(Sachs et al, , 2011Okubo et al, 2012).…”

Preferential Association of Endophytic Bradyrhizobia with Different Rice Cultivars and Its Implications for Rice Endophyte Evolution

“…A preliminary experiment by Okubo et al (45) showed that a photosynthetic gene cluster was detected in the genome of nonsymbiotic Bradyrhizobium strain S23321 that displayed high sim-ilarity to the A. indica symbionts, whereas the phylogenetic tree of the 16S rRNA gene was closely related to that of B. diazoefficiens USDA110. These observations may also support our hypothesis that environmental conditions and/or habitat have been continuously driving the evolution of the plant-bradyrhizobium interaction.…”