Culture‐independent characterization of a novel magnetotactic member affiliated to the Beta class of the Proteobacteria phylum from an acidic lagoon

Abstract

Magnetotactic bacteria (MTB) comprise a group of motile microorganisms common in most mesothermal aquatic habitats with pH values around neutrality. However, during the last two decades, a number of MTB from extreme environments have been characterized including: cultured alkaliphilic strains belonging to the Deltaproteobacteria class of the Proteobacteria phylum; uncultured moderately thermophilic strains belonging to the Nitrospirae phylum; cultured and uncultured moderately halophilic or strongly halotolerant bacteria affiliated with the Deltaproteobacteria and Gammaproteobacteria classes and an uncultured psychrophilic species belonging to the Alphaproteobacteria class. Here, we used culture-independent techniques to characterize MTB from an acidic freshwater lagoon in Brazil (pH ∼ 4.4). MTB morphotypes found in this acidic lagoon included cocci, rods, spirilla and vibrioid cells. Magnetite (Fe O ) was the only mineral identified in magnetosomes of these MTB while magnetite magnetosome crystal morphologies within the different MTB cells included cuboctahedral (present in spirilla), elongated prismatic (present in cocci and vibrios) and bullet-shaped (present in rod-shaped cells). Intracellular pH measurements using fluorescent dyes showed that the cytoplasmic pH was close to neutral in most MTB cells and acidic in some intracellular granules. Based on 16S rRNA gene phylogenetic analyses, some of the retrieved gene sequences belonged to the genus Herbaspirillum within the Betaproteobacteria class of the Proteobacteria phylum. Fluorescent in situ hybridization using a Herbaspirillum-specific probe hybridized with vibrioid MTB in magnetically-enriched samples. Transmission electron microscopy of the Herbaspirillum-like MTB revealed the presence of many intracellular granules and a single chain of elongated prismatic magnetite magnetosomes. Diverse populations of MTB have not seemed to have been described in detail in an acid environment. In addition, this is the first report of an MTB phylogenetically affiliated with Betaproteobacteria class.

Magnetosome magnetite biomineralization in a flagellated protist: evidence for an early evolutionary origin for magnetoreception in eukaryotes

“…Phylogenetically, MTB are extremely diverse. Representatives of this group are present in a number of phyla including several classes of the Proteobacteria (Sakaguchi et al ., ; Lefèvre et al ., ; Morillo et al ., ; Taoka et al ., ; Abreu et al ., ), the Nitrospirae (Lefèvre et al ., ; Lin et al ., ) and the candidate phylum Omnitrophica (Kolinko et al ., , ). Culture‐independent methods and single‐cell genome analysis indicate that the diversity and phylogenetic distribution of magnetotactic organisms are underestimated (Kolinko et al ., ; Rinke et al ., ) and may extend to other phylogenetic groups including the phyla Latescibacteria and Planctomycetes (Lin and Pan, ; Lin et al ., ; Lin et al ., ) or maybe even other domains of life (Torres de Araujo et al ., ).…”

Expanding magnetic organelle biogenesis in the domainBacteria

“…Unexpectedly, we find living MTB cells in acidic peatland soils (pH 4.3-5.7) with high water contents (>60%) and organic matter contents (typically >20%) 42–44 . MTB have been found broadly in diverse aquatic ecosystems 17 , including some extreme environments such as hot springs 45,46 , saline-alkaline lakes 47 , acidic lagoons and mine drainage systems 33,48 , and deep-sea sediments 49 , but reports of MTB in soils are limited to a few studies that were published almost 30 years ago 18,19 . Whether MTB can survive and reproduce in waterlogged soil environments remains unresolved, and the taxonomic diversity of MTB in these environments has not been elucidated.…”

“…In recent years, the known extent of MTB diversity has undergone a significant expansion due to methodological advances, such as the successful cultivation of novel MTB strains e.g., 29–32 , 16S rRNA gene-based characterization e.g., 33–35 , genome mining of public repositories including GenBank and IMG/ER 17,36 , and cultivation-independent surveys of magnetosome gene clusters (MGCs, which are physically clustered groups of genes that are together responsible for magnetosomal biogenesis) 37,38 . MTB have now been further identified in other Bacterial taxa, including the Betaproteobacteria , Zetaproteobacteria , “ Candidatus Etaproteobacteria”, and “ Candidatus Lambdaproteobacteria” classes of the Proteobacteria phylum, the candidate phylum Omnitrophica (previously known as the candidate division OP3), the candidate phylum Latescibacteria (previously known as the candidate division WS3), and the phylum Planctomycetes , according to the NCBI taxonomy.…”

Biomineralization of Magnetosomes: Billion-Year Evolution Shaping Modern Nanotools

“…Mam and Mms protein functions involved in MB are described in The advances of molecular biology techniques provided a much greater understanding of the MB mechanism over the last years as cultured and environmental MTB had their genomes sequenced. Magnetite MGCs and magnetite magnetosomes were studied in magnetotactic proteobacteria affiliated to the classes Alpha- [32][33][34][35][36], Beta- [37], Gamma- [38,39], Delta- [40][41][42][43], Ca. Eta- [9,32,44,45], Ca.…”