Cultivation‐independent characterization of ‘Candidatus Magnetobacterium bavaricum’ via ultrastructural, geochemical, ecological and metagenomic methods

Abstract

'Candidatus Magnetobacterium bavaricum' is unusual among magnetotactic bacteria (MTB) in terms of cell size (8-10 µm long, 1.5-2 µm in diameter), cell architecture, magnetotactic behaviour and its distinct phylogenetic position in the deep-branching Nitrospira phylum. In the present study, improved magnetic enrichment techniques permitted high-resolution scanning electron microscopy and energy dispersive X-ray analysis, which revealed the intracellular organization of the magnetosome chains. Sulfur globule accumulation in the cytoplasm point towards a sulfur-oxidizing metabolism of 'Candidatus M. bavaricum'. Detailed analysis of 'Candidatus M. bavaricum' microhabitats revealed more complex distribution patterns than previously reported, with cells predominantly found in low oxygen concentration. No correlation to other geochemical parameters could be observed. In addition, the analysis of a metagenomic fosmid library revealed a 34 kb genomic fragment, which contains 33 genes, among them the complete rRNA gene operon of 'Candidatus M. bavaricum' as well as a gene encoding a putative type IV RubisCO large subunit.

Genomic insights into the uncultured genus ‘Candidatus Magnetobacterium’ in the phylum Nitrospirae

“…In combination with the results of previous microhabitat study (Jogler et al, 2010), the genomic analysis presented here has allowed us to predict the ecology of 'Ca. Magnetobacterium' genus.…”

“…Coexistence of different autotrophic pathways has been reported in some microorganisms (Markert et al, 2007), thus it is also possible for Mcas conduct rTCA pathway for CO 2 fixation, although this needs further experimental determination. Similar to Mbav (Jogler et al, 2010), a form IV ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) encoding gene (Peg.1181) was identified in the genome. However, the lack of carboxylase and oxygenase activity of this gene suggests that Calvin-Benson-Bassham pathway for CO 2 fixation should not operate in Mcas.…”

“…Members of 'Ca. Magnetobacterium' genus are known to live near microoxic to anoxic layers (Jogler et al, 2010), suggesting they being occasionally exposed to oxygen. Accordingly, Mcas contains genes encoding aa 3 -type cytochrome oxidases that may allow adaptation to microoxic conditions.…”

“…Recent studies have suggested that these organisms may be capable of oxidizing sulfur (Spring and Bazylinski, 2006;Jogler et al, 2010), thus linking this genus to the key steps of iron and sulfur cycles in nature. However, except for a few short genomic fragments (Jogler et al, 2010;Jogler et al, 2011;Lin et al, 2011), very little genetic data of this genus are available owing to their unculturability. Consequently, knowledge of their trophic strategy, physiology and intracellular biomineralization remains very limited.…”

“…Originally discovered through electron microscope observation and ribosomal RNA gene sequencing (Vali et al, 1987;Spring et al, 1993), the Nitrospirae MTB are found to be widespread in aquatic environments and sometimes even account for a significant proportion (up to 30%) of microbial biomass in the microhabitats (Spring et al, 1993;Lin et al, 2014). Recent studies have suggested that these organisms may be capable of oxidizing sulfur (Spring and Bazylinski, 2006;Jogler et al, 2010), thus linking this genus to the key steps of iron and sulfur cycles in nature. However, except for a few short genomic fragments (Jogler et al, 2010;Jogler et al, 2011;Lin et al, 2011), very little genetic data of this genus are available owing to their unculturability.…”