Abstract
Members of the phylum Acidobacteria are ubiquitous in various environments. Soil acidobacteria have been reported to present a variety of strategies for their success in terrestrial environments. However, owing to lack of pure culture, information on animal-associated acidobacteria are limited, except for those obtained from 16S rRNA genes. To date, only two acidobacteria have been isolated from animals, namely strain M133T obtained from coral Porites lutea and Acanthopleuribacter pedis KCTC 12899T isolated from chiton. Genomics and physiological characteristics of strain M133T and A. pedis KCTC 12899T were compared with 19 other isolates (one strain from each genus) in the phylum Acidobacteria. The results revealed that strain M133T represents a new species in a new genus in the family Acanthopleuribacteraceae. To date, these two Acanthopleuribacteraceae isolates have the largest genomes (10.85–11.79 Mb) in the phylum Acidobacteria. Horizontal gene transfer and gene duplication influenced the structure and plasticity of these large genomes. Dissimilatory nitrate reduction and abundant secondary metabolite biosynthetic gene clusters (including eicosapentaenoic acid de novo biosynthesis) are two distinct features of the Acanthopleuribacteraceae bacteria in the phylum Acidobacteria. The absence of glycoside hydrolases involved in plant polysaccharide degradation and presence of animal disease-related peptidases indicate that these bacteria have evolved to adapt to the animal hosts. In addition to low- and high-affinity respiratory oxygen reductases, enzymes for nitrate to nitrogen, and sulfhydrogenase were also detected in strain M133T, suggesting the capacity and flexibility to grow in aerobic and anaerobic environments. This study highlighted the differences in genome structure, carbohydrate and protein utilization, respiration, and secondary metabolism between animal-associated acidobacteria and other acidobacteria, especially the soil acidobacteria, displaying flexibility and versatility of the animal-associated acidobacteria in environmental adaption.
Highlights
The results indicate that biosynthetic gene clusters (BGCs) are as large as genomic islands (GIs) in strain M133T (Figure 1) and A. pedis Korean Collection for Type Cultures (KCTC) 12899T, accounting for 22.6% and 20% of the genome, respectively (Table 1)
Species belonging to phylum Acidobacteria are ubiquitous among animals, yet their ecological role remains unclear
Comparative genomic and high-throughput sequencing analyses indicated that Acanthopleuribacteraceae is a distinct branch of the phylum Acidobacteria, features a large genome that harbors genes associated with secondary metabolic production, tolerance to oxygen fluctuation, and intimate animal association
Summary
Bacteria belonging to the phylum “Acidobacteria” are ubiquitous in various environments, including freshwater mud (Liesack et al, 1994; Zimmermann et al, 2012), hot spring microbial mats (Losey et al, 2013), metal-rich acidic waters (Falagán et al, 2017), various soils (Barns et al, 1999; Quaiser et al, 2003; Chanal et al, 2006; Vieira et al, 2017; Kalam et al, 2020), and animals (O’Connor-Sánchez et al, 2014; Liang et al, 2017; Laport et al, 2019). To date, Acanthopleuribacter pedis KCTC 12899T is the only described acidobacterium isolated from animals (chiton) (Fukunaga et al, 2008). Another acidobacterial isolate, strain M133T, was isolated from stony coral Porites lutea. This study aimed to identify the animalassociated characteristics of acidobacteria using comparative genomic and high-throughput sequencing analyses based on these two strains
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