Abstract

BackgroundMicrobial communities recurrently establish metabolic associations resulting in increased fitness and ability to perform complex tasks, such as xenobiotic degradation. In a previous study, we have described a sulfonamide-degrading consortium consisting of a novel low-abundant actinobacterium, named strain GP, and Achromobacter denitrificans PR1. However, we found that strain GP was unable to grow independently and could not be further purified.ResultsPrevious studies suggested that strain GP might represent a new putative species within the Leucobacter genus (16S rRNA gene similarity < 97%). In this study, we found that average nucleotide identity (ANI) with other Leucobacter spp. ranged between 76.8 and 82.1%, further corroborating the affiliation of strain GP to a new provisional species. The average amino acid identity (AAI) and percentage of conserved genes (POCP) values were near the lower edge of the genus delimitation thresholds (65 and 55%, respectively). Phylogenetic analysis of core genes between strain GP and Leucobacter spp. corroborated these findings. Comparative genomic analysis indicates that strain GP may have lost genes related to tetrapyrrole biosynthesis and thiol transporters, both crucial for the correct assembly of cytochromes and aerobic growth. However, supplying exogenous heme and catalase was insufficient to abolish the dependent phenotype. The actinobacterium harbors at least two copies of a novel genetic element containing a sulfonamide monooxygenase (sadA) flanked by a single IS1380 family transposase. Additionally, two homologs of sadB (4-aminophenol monooxygenase) were identified in the metagenome-assembled draft genome of strain GP, but these were not located in the vicinity of sadA nor of mobile or integrative elements.ConclusionsComparative genomics of the genus Leucobacter suggested the absence of some genes encoding for important metabolic traits in strain GP. Nevertheless, although media and culture conditions were tailored to supply its potential metabolic needs, these conditions were insufficient to isolate the PR1-dependent actinobacterium further. This study gives important insights regarding strain GP metabolism; however, gene expression and functional studies are necessary to characterize and further isolate strain GP. Based on our data, we propose to classify strain GP in a provisional new species within the genus Leucobacter, ‘Candidatus Leucobacter sulfamidivorax‘.

Highlights

  • Microbial communities recurrently establish metabolic associations resulting in increased fitness and ability to perform complex tasks, such as xenobiotic degradation

  • Flagella have not been previously reported for the type strain of A. denitrificans, their presence has been repeatedly observed in other strains from this species [27] and other species of the Achromobacter genus [28, 29]

  • The number of genes and the genome size of this strain was similar to the ones found in other members of the Leucobacter genus (Table 2). These results suggest that, despite the PR1-dependent phenotype, strain GP differs from obligate parasites that, in the process of adapting to their hosts, undergo a process called reductive genome evolution, which results in relatively small genomes [66, 67]. (Table 3) Comparative genomic analysis of the Leucobacter genus revealed that the pangenome consists of 12,998 orthologous gene clusters

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Summary

Introduction

Microbial communities recurrently establish metabolic associations resulting in increased fitness and ability to perform complex tasks, such as xenobiotic degradation. Microbial communities are known to establish sophisticated metabolic interactions in order to achieve complex and energy-expensive tasks [1,2,3,4,5] These syntrophic relationships are frequently studied in bacterial pathogens and symbiotic bacteria, where the interaction with the host often drives progressive adaptation, mutation, and subsequently, gene loss. The phenomena underlying metabolic cooperation and competition within environmental communities are often more complex, and their implications for microbial ecology are still poorly understood [5, 11] These communities recurrently exchange metabolites or co-factors and are often associated with xenobiotic-degraders thriving in polluted environments [5, 11,12,13,14,15]. We have described a microbial consortium between Achromobacter denitrificans strain PR1 and strain

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