scholarly journals Expanding magnetic organelle biogenesis in the domain Bacteria

Microbiome ◽  
2020 ◽  
Vol 8 (1) ◽  
Author(s):  
Wei Lin ◽  
Wensi Zhang ◽  
Greig A. Paterson ◽  
Qiyun Zhu ◽  
Xiang Zhao ◽  
...  

Abstract Background The discovery of membrane-enclosed, metabolically functional organelles in Bacteria has transformed our understanding of the subcellular complexity of prokaryotic cells. Biomineralization of magnetic nanoparticles within magnetosomes by magnetotactic bacteria (MTB) is a fascinating example of prokaryotic organelles. Magnetosomes, as nano-sized magnetic sensors in MTB, facilitate cell navigation along the local geomagnetic field, a behaviour referred to as magnetotaxis or microbial magnetoreception. Recent discovery of novel MTB outside the traditionally recognized taxonomic lineages suggests that MTB diversity across the domain Bacteria are considerably underestimated, which limits understanding of the taxonomic distribution and evolutionary origin of magnetosome organelle biogenesis. Results Here, we perform the most comprehensive metagenomic analysis available of MTB communities and reconstruct metagenome-assembled MTB genomes from diverse ecosystems. Discovery of MTB in acidic peatland soils suggests widespread MTB occurrence in waterlogged soils in addition to subaqueous sediments and water bodies. A total of 168 MTB draft genomes have been reconstructed, which represent nearly a 3-fold increase over the number currently available and more than double the known MTB species at the genome level. Phylogenomic analysis reveals that these genomes belong to 13 Bacterial phyla, six of which were previously not known to include MTB. These findings indicate a much wider taxonomic distribution of magnetosome organelle biogenesis across the domain Bacteria than previously thought. Comparative genome analysis reveals a vast diversity of magnetosome gene clusters involved in magnetosomal biogenesis in terms of gene content and synteny residing in distinct taxonomic lineages. Phylogenetic analyses of core magnetosome proteins in this largest available and taxonomically diverse dataset support an unexpectedly early evolutionary origin of magnetosome biomineralization, likely ancestral to the origin of the domain Bacteria. Conclusions These findings expand the taxonomic and phylogenetic diversity of MTB across the domain Bacteria and shed new light on the origin and evolution of microbial magnetoreception. Potential biogenesis of the magnetosome organelle in the close descendants of the last bacterial common ancestor has important implications for our understanding of the evolutionary history of bacterial cellular complexity and emphasizes the biological significance of the magnetosome organelle.

2020 ◽  
Author(s):  
Wei Lin ◽  
Wensi Zhang ◽  
Greig A. Paterson ◽  
Qiyun Zhu ◽  
Xiang Zhao ◽  
...  

AbstractThe discovery of membrane-enclosed, metabolically functional organelles in Bacteria and Archaea has transformed our understanding of the subcellular complexity of prokaryotic cells. However, whether prokaryotic organelles emerged early or late in evolutionary history remains unclear and limits understanding of the nature and cellular complexity of early life. Biomineralization of magnetic nanoparticles within magnetosomes by magnetotactic bacteria (MTB) is a fascinating example of prokaryotic organelles. Here, we reconstruct 168 metagenome-assembled MTB genomes from various aquatic environments and waterlogged soils. These genomes represent nearly a 3-fold increase over the number currently available, and more than double the known MTB species. Phylogenomic analysis reveals that these newly described genomes belong to 13 Bacterial phyla, six of which were previously not known to include MTB. These findings indicate a much wider taxonomic distribution of magnetosome organelle biogenesis across the domain Bacteria than previously thought. Comparative genome analysis reveals a vast diversity of magnetosome gene clusters involved in magnetosomal biogenesis in terms of gene content and synteny residing in distinct taxonomic lineages. These gene clusters therefore represent a promising, diverse genetic resource for biosynthesizing novel magnetic nanoparticles. Finally, our phylogenetic analyses of the core magnetosome proteins in this largest available and taxonomically diverse dataset support an unexpectedly early evolutionary origin of magnetosome biomineralization, likely ancestral to the origin of the domain Bacteria. These findings emphasize the potential biological significance of prokaryotic organelles on the early Earth and have important implications for our understanding of the evolutionary history of cellular complexity.


2017 ◽  
Author(s):  
Migun Shakya ◽  
Shannon M. Soucy ◽  
Olga Zhaxybayeva

AbstractSeveral bacterial and archaeal lineages produce nanostructures that morphologically resemble small tailed viruses, but, unlike most viruses, contain apparently random pieces of the host genome. Since these elements can deliver the packaged DNA to other cells, they were dubbed Gene Transfer Agents (GTAs). Because many genes involved in GTA production have viral homologs, it has been hypothesized that the GTA ancestor was a virus. Whether GTAs represent an atypical virus, a defective virus, or a virus co-opted by the prokaryotes for some function, remains to be elucidated. To evaluate these possibilities, we examined the distribution and evolutionary histories of genes that encode a GTA in the α-proteobacteriumRhodobacter capsulatus(RcGTA). We report that although homologs of many individual RcGTA genes are abundant across bacteria and their viruses, RcGTA-like genomes are mainly found in one subclade of α-proteobacteria. When compared to the viral homologs, genes of the RcGTA-like genomes evolve significantly slower, and do not have higher %A+T nucleotides than their host chromosomes. Moreover, they appear to reside in stable regions of the bacterial chromosomes that are generally conserved across taxonomic orders. These findings argue against RcGTA being an atypical or a defective virus. Our phylogenetic analyses suggest that RcGTA ancestor likely originated in the lineage that gave rise to contemporary α-proteobacterial ordersRhizobiales, Rhodobacterales, Caulobacterales, Parvularculales, and Sphingomonadales,and since that time the RcGTA-like element has co-evolved with its host chromosomes. Such evolutionary history is compatible with maintenance of these elements by bacteria due to some selective advantage. As for many other prokaryotic traits, horizontal gene transfer played a substantial role in the evolution of RcGTA-like elements, not only in shaping its genome components within the orders, but also in occasional dissemination of RcGTA-like regions across the orders and even to different bacterial phyla.


2020 ◽  
Vol 12 (10) ◽  
pp. 1830-1840
Author(s):  
Xiangchen Li ◽  
Jian Cheng ◽  
Xiaonan Liu ◽  
Xiaoxian Guo ◽  
Yuqian Liu ◽  
...  

Abstract Fusidane-type antibiotics represented by fusidic acid, helvolic acid, and cephalosporin P1 have very similar core structures, but they are produced by fungi belonging to different taxonomic groups. The origin and evolution of fusidane-type antibiotics biosynthetic gene clusters (BGCs) in different antibiotics producing strains remained an enigma. In this study, we investigated the distribution and evolution of the fusidane BGCs in 1,284 fungal genomes. We identified 12 helvolic acid BGCs, 4 fusidic acid BGCs, and 1 cephalosporin P1 BGC in Pezizomycotina fungi. Phylogenetic analyses indicated six horizontal gene transfer (HGT) events in the evolutionary trajectory of the BGCs, including 1) three transfers across Eurotiomycetes and Sordariomycetes classes; 2) one transfer between genera under Sordariomycetes class; and 3) two transfers within Aspergillus genus under Eurotiomycetes classes. Finally, we proposed that the ancestor of fusidane BGCs would be originated from the Zoopagomycota by ancient HGT events according to the phylogenetic trees of key enzymes in fusidane BGCs (OSC and P450 genes). Our results extensively clarify the evolutionary trajectory of fusidane BGCs by HGT among distantly related fungi and provide new insights into the evolutionary mechanisms of metabolic pathways in fungi.


Author(s):  
Runjia Ji ◽  
Wensi Zhang ◽  
Yongxin Pan ◽  
Wei Lin

Magnetosome gene clusters (MGCs), which are responsible for magnetosome biosynthesis and organization in magnetotactic bacteria (MTB), are the key to deciphering the mechanisms and evolutionary origin of magnetoreception, organelle biogenesis, and intracellular biomineralization in bacteria. Here, we report the development of MagCluster, a Python stand-alone tool for efficient exploration of MGCs from large-scale (meta)genomic data.


Toxins ◽  
2019 ◽  
Vol 11 (5) ◽  
pp. 269 ◽  
Author(s):  
Lian Qin ◽  
Xiaoxing Zhang ◽  
Xiaoguo Chen ◽  
Ke Wang ◽  
Yitian Shen ◽  
...  

The mlr-dependent biodegradation plays an essential role in the natural attenuation of microcystins (MCs) in eutrophic freshwater ecosystems. However, their evolutionary origin is still unclear due to the lack of mlr gene cluster sequences. In this study, a Sphingopyxis sp. strain X20 with high MC-degrading ability was isolated, and the mlrA gene activity was verified by heterologous expression. The whole sequence of the mlr gene cluster in strain X20 was obtained through PCR and thermal asymmetric interlaced (TAIL)-PCR, and then used for evolutionary origin analyses together with the sequences available in GenBank. Phylogenetic analyses of mlr gene clusters suggested that the four mlr genes had the same origin and evolutionary history. Genomic island analyses showed that there is a genomic island on the genome of sphingomonads that is capable of degrading MCs, on which the mlr gene cluster anchors. The concentrated distribution of the mlr gene cluster in sphingomonads implied that these genes have likely been present in the sphingomonads gene pool for a considerable time. Therefore, the mlr gene cluster may have initially entered into the genome of sphingomonads together with the genomic island by a horizontal gene transfer event, and then become inherited by some sphingomonads. The species other than sphingomonads have likely acquired mlr genes from sphingomonads by recently horizontal gene transfer due to the sporadic distribution of MC-degrading species and the mlr genes in them. Our results shed new light on the evolutionary origin of the mlr cluster and thus facilitate the interpretation of characteristic distribution of the mlr gene in bacteria and the understanding of whole mlr pathway.


2009 ◽  
Vol 75 (17) ◽  
pp. 5676-5686 ◽  
Author(s):  
Kohjiro Tanaka ◽  
Seiichi Furukawa ◽  
Naruo Nikoh ◽  
Tetsuhiko Sasaki ◽  
Takema Fukatsu

ABSTRACT Wolbachia endosymbionts are ubiquitously found in diverse insects including many medical and hygienic pests, causing a variety of reproductive phenotypes, such as cytoplasmic incompatibility, and thereby efficiently spreading in host insect populations. Recently, Wolbachia-mediated approaches to pest control and management have been proposed, but the application of these approaches has been hindered by the lack of genetic transformation techniques for symbiotic bacteria. Here, we report the genome and structure of active bacteriophages from a Wolbachia endosymbiont. From the Wolbachia strain wCauB infecting the moth Ephestia kuehniella two closely related WO prophages, WOcauB2 of 43,016 bp with 47 open reading frames (ORFs) and WOcauB3 of 45,078 bp with 46 ORFs, were characterized. In each of the prophage genomes, an integrase gene and an attachment site core sequence were identified, which are putatively involved in integration and excision of the mobile genetic elements. The 3′ region of the prophages encoded genes with sequence motifs related to bacterial virulence and protein-protein interactions, which might represent effector molecules that affect cellular processes and functions of their host bacterium and/or insect. Database searches and phylogenetic analyses revealed that the prophage genes have experienced dynamic evolutionary trajectories. Genes similar to the prophage genes were found across divergent bacterial phyla, highlighting the active and mobile nature of the genetic elements. We suggest that the active WO prophage genomes and their constituent sequence elements would provide a clue to development of a genetic transformation vector for Wolbachia endosymbionts.


2003 ◽  
Vol 77 (13) ◽  
pp. 7202-7213 ◽  
Author(s):  
Marco Salemi ◽  
Tulio De Oliveira ◽  
Valerie Courgnaud ◽  
Vincent Moulton ◽  
Barbara Holland ◽  
...  

ABSTRACT To clarify the origin and evolution of the primate lentiviruses (PLVs), which include human immunodeficiency virus types 1 and 2 as well as their simian relatives, simian immunodeficiency viruses (SIVs), isolated from several host species, we investigated the phylogenetic relationships among the six supposedly nonrecombinant PLV lineages for which the full genome sequences are available. Employing bootscanning as an exploratory tool, we located several regions in the PLV genome that seem to have uncertain or conflicting phylogenetic histories. Phylogeny reconstruction based on distance and maximum-likelihood algorithms followed by a number of statistical tests confirms the existence of at least five putative recombinant fragments in the PLV genome with different clustering patterns. Split decomposition analysis also shows that phylogenetic relationships among PLVs may be better represented by network-based graphs, such as the ones produced by SplitsTree. Our findings not only imply that the six so-called pure PLV lineages have in fact mosaic genomes but also make more unlikely the hypothesis of cospeciation of SIVs and their simian hosts.


2021 ◽  
Vol 17 (7) ◽  
pp. e1009730
Author(s):  
Jialu Zheng ◽  
Jianhua Wang ◽  
Zhen Gong ◽  
Guan-Zhu Han

The ancestor of cetaceans underwent a macroevolutionary transition from land to water early in the Eocene Period >50 million years ago. However, little is known about how diverse retroviruses evolved during this shift from terrestrial to aquatic environments. Did retroviruses transition into water accompanying their hosts? Did retroviruses infect cetaceans through cross-species transmission after cetaceans invaded the aquatic environments? Endogenous retroviruses (ERVs) provide important molecular fossils for tracing the evolution of retroviruses during this macroevolutionary transition. Here, we use a phylogenomic approach to study the origin and evolution of ERVs in cetaceans. We identify a total of 8,724 ERVs within the genomes of 25 cetaceans, and phylogenetic analyses suggest these ERVs cluster into 315 independent lineages, each of which represents one or more independent endogenization events. We find that cetacean ERVs originated through two possible routes. 298 ERV lineages may derive from retrovirus endogenization that occurred before or during the transition from land to water of cetaceans, and most of these cetacean ERVs were reaching evolutionary dead-ends. 17 ERV lineages are likely to arise from independent retrovirus endogenization events that occurred after the split of mysticetes and odontocetes, indicating that diverse retroviruses infected cetaceans through cross-species transmission from non-cetacean mammals after the transition to aquatic life of cetaceans. Both integration time and synteny analyses support the recent or ongoing activity of multiple retroviral lineages in cetaceans, some of which proliferated into hundreds of copies within the host genomes. Although ERVs only recorded a proportion of past retroviral infections, our findings illuminate the complex evolution of retroviruses during one of the most marked macroevolutionary transitions in vertebrate history.


Author(s):  
Yang Liu ◽  
Tao Pei ◽  
Juan Du ◽  
Meijie Chao ◽  
Ming-Rong Deng ◽  
...  

A novel Gram-stain-negative, facultatively anaerobic, rod-shaped and non-motile bacterial strain, designated as 4C16AT, was isolated from a tidal flat sediment and characterized by using a polyphasic taxonomic approach. Strain 4C16AT was found to grow at 10–40 °C (optimum, 28 °C), at pH 5.0–10.0 (optimum, pH 6.0–7.0) and in 0–6 % (w/v) NaCl (optimum, 1 %). Phylogenetic analysis based on 16S rRNA gene sequences revealed that strain 4C16AT fell into the genus Roseibium , and shared the highest identity of 98.9 % with the closest type strain Roseibium suaedae KACC 13772T and less than 98.0 % identity with other type strains of recognized species within this genus. The phylogenomic analysis indicated that strain 4C16AT formed an independent branch within this genus. The 28.6 % digital DNA–DNA hybridization estimate and 85.0 % average nucleotide identity between strains 4C16AT and R. suaedae KACC 13772T were the highest, but still far below their respective threshold for species definition, implying that strain 4C16AT should represent a novel genospecies. The predominant cellular fatty acid was summed feature 8; the polar lipids were diphosphatidylglycerol, phosphatidylcholine, phosphatidylethanolamine, phosphatidylglycerol and phosphatidylmonomethylethanolamine; the respiratory quinones were Q-9 and Q-10. The genomic DNA G+C content was 59.8mol %. Based on phylogenetic analyses and phenotypic and chemotaxonomic characteristics, strain 4C16AT is concluded to represent a novel species of the genus Roseibium , for which the name Roseibium litorale sp. nov. is proposed. The type strain of the species is 4C16AT (=GDMCC 1.1932T=KACC 22078T). We also propose the reclassification of Labrenzia polysiphoniae as Roseibium polysiphoniae comb. nov. and ‘Labrenzia callyspongiae’ as Roseibium callyspongiae sp. nov.


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