scholarly journals Multiple evolutionary origins reflect the importance of sialic acid transporters in the colonization potential of bacterial pathogens and commensals

2021 ◽  
Vol 7 (6) ◽  
Author(s):  
Emmanuele Severi ◽  
Michelle Rudden ◽  
Andrew Bell ◽  
Tracy Palmer ◽  
Nathalie Juge ◽  
...  

Located at the tip of cell surface glycoconjugates, sialic acids are at the forefront of host–microbe interactions and, being easily liberated by sialidase enzymes, are used as metabolites by numerous bacteria, particularly by pathogens and commensals living on or near diverse mucosal surfaces. These bacteria rely on specific transporters for the acquisition of host-derived sialic acids. Here, we present the first comprehensive genomic and phylogenetic analysis of bacterial sialic acid transporters, leading to the identification of multiple new families and subfamilies. Our phylogenetic analysis suggests that sialic acid-specific transport has evolved independently at least eight times during the evolution of bacteria, from within four of the major families/superfamilies of bacterial transporters, and we propose a robust classification scheme to bring together a myriad of different nomenclatures that exist to date. The new transporters discovered occur in diverse bacteria, including Spirochaetes , Bacteroidetes , Planctomycetes and Verrucomicrobia , many of which are species that have not been previously recognized to have sialometabolic capacities. Two subfamilies of transporters stand out in being fused to the sialic acid mutarotase enzyme, NanM, and these transporter fusions are enriched in bacteria present in gut microbial communities. Our analysis supports the increasing experimental evidence that competition for host-derived sialic acid is a key phenotype for successful colonization of complex mucosal microbiomes, such that a strong evolutionary selection has occurred for the emergence of sialic acid specificity within existing transporter architectures.

2021 ◽  
Author(s):  
Emmanuele Severi ◽  
Michelle Rudden ◽  
Andrew Bell ◽  
Tracy Palmer ◽  
Nathalie Juge ◽  
...  

AbstractLocated at the tip of cell surface glycoconjugates, sialic acids are at the forefront of host-microbe interactions and, being easily liberated by sialidase enzymes, are used as metabolites by numerous bacteria, particularly by pathogens and commensals living on or near diverse mucosal surfaces. These bacteria rely on specific transporters for the acquisition of host-derived sialic acids. Here, we present the first comprehensive genomic and phylogenetic analysis of bacterial sialic acid transporters, leading to the identification of multiple new families and subfamilies. Our phylogenetic analysis suggests that sialic acid-specific transport has evolved independently at least 8 times during the evolution of bacteria, from within 4 of the major families/superfamilies of bacterial transporters, and we propose a robust classification scheme to bring together a myriad of different nomenclatures that exist to date. The new transporters discovered occur in diverse bacteria including Spirochaetes, Bacteroidetes, Planctomycetes, and Verrucomicrobia, many of which are species that have not been previously recognised to have sialometabolic capacities. Two subfamilies of transporters stand out in being fused to the sialic acid mutarotase enzyme, NanM, and these transporter fusions are enriched in bacteria present in gut microbial communities. We also provide evidence for a possible function of a sialic acid transporter component in chemotaxis that is independent of transport. Our analysis supports the increasing experimental evidence that competition for host-derived sialic acid is a key phenotype for successful colonisation of complex mucosal microbiomes, such that a strong evolutionary selection has occurred for the emergence of sialic acid specificity within existing transporter architectures.


2016 ◽  
Vol 198 (20) ◽  
pp. 2803-2809 ◽  
Author(s):  
Ariel Rangel ◽  
Susan M. Steenbergen ◽  
Eric R. Vimr

ABSTRACTThe sialic acids (N-acylneuraminates) are a group of nine-carbon keto-sugars existing mainly as terminal residues on animal glycoprotein and glycolipid carbohydrate chains. Bacterial commensals and pathogens exploit host sialic acids for nutrition, adhesion, or antirecognition, whereN-acetyl- orN-glycolylneuraminic acids are the two predominant chemical forms of sialic acids. Each form may be modified by acetyl esters at carbon position 4, 7, 8, or 9 and by a variety of less-common modifications. Modified sialic acids produce challenges for colonizing bacteria, because the chemical alterations toN-acetylneuraminic acid (Neu5Ac) confer increased resistance to sialidase and aldolase activities essential for the catabolism of host sialic acids. Bacteria withO-acetyl sialate esterase(s) utilize acetylated sialic acids for growth, thereby gaining a presumed metabolic advantage over competitors lacking this activity. Here, we demonstrate the esterase activity ofEscherichia coliNanS after purifying it as a C-terminal HaloTag fusion. Using a similar approach, we show thatE. colistrain O157:H7 Stx prophage or prophage remnants invariably include paralogs ofnanSoften located downstream of the Shiga-like toxin genes. These paralogs may include sequences encoding N- or C-terminal domains of unknown function where the NanS domains can act as sialateO-acetyl esterases, as shown by complementation of anE. colistrain K-12nanSmutant and the unimpaired growth of anE. coliO157nanSmutant onO-acetylated sialic acid. We further demonstrate thatnanShomologs inStreptococcusspp. also encode active esterase, demonstrating an unexpected diversity of bacterial sialateO-acetyl esterase.IMPORTANCEThe sialic acids are a family of over 40 naturally occurring 9-carbon keto-sugars that function in a variety of host-bacterium interactions. These sugars occur primarily as terminal carbohydrate residues on host glycoproteins and glycolipids. Available evidence indicates that diverse bacterial species use host sialic acids for adhesion or as sources of carbon and nitrogen. Our results show that the catabolism of the diacetylated form of host sialic acid requires a specialized esterase, NanS. Our results further show thatnanShomologs exist in bacteria other thanEscherichia coli, as well as part of toxigenicE. coliprophage. The unexpected diversity of these enzymes suggests new avenues for investigating host-bacterium interactions. Therefore, these original results extend our previous studies ofnanSto include mucosal pathogens, prophage, and prophage remnants. This expansion of thenanSsuperfamily suggests important, although as-yet-unknown, functions in host-microbe interactions.


Microbiology ◽  
2020 ◽  
Vol 166 (3) ◽  
pp. 262-277 ◽  
Author(s):  
Meagan Leah Cohen ◽  
Ekaterina Vadimovna Mashanova ◽  
Sveta Vivian Jagannathan ◽  
William Soto

Many microorganisms engaged in host-microbe interactions pendulate between a free-living phase and a host-affiliated stage. How adaptation to stress during the free-living phase affects host-microbe associations is unclear and understudied. To explore this topic, the symbiosis between Hawaiian bobtail squid (Euprymna scolopes) and the luminous bacterium Vibrio fischeri was leveraged for a microbial experimental evolution study. V. fischeri experienced adaptation to extreme pH while apart from the squid host. V. fischeri was serially passaged for 2000 generations to the lower and upper pH growth limits for this microorganism, which were pH 6.0 and 10.0, respectively. V. fischeri was also serially passaged for 2000 generations to vacillating pH 6.0 and 10.0. Evolution to pH stress both facilitated and impaired symbiosis. Microbial evolution to acid stress promoted squid colonization and increased bioluminescence for V. fischeri , while symbiont adaptation to alkaline stress diminished these two traits. Oscillatory selection to acid and alkaline stress also improved symbiosis for V. fischeri , but the facilitating effects were less than that provided by microbial adaptation to acid stress. In summary, microbial adaptation to harsh environments amid the free-living phase may impact the evolution of host-microbe interactions in ways that were not formerly considered.


2015 ◽  
Vol 65 (Pt_5) ◽  
pp. 1537-1541 ◽  
Author(s):  
De-Chao Zhang ◽  
Rosa Margesin

A Gram-stain-negative, Na+-requiring bacterial strain, designated B20-1T, was isolated from soil of the root system of mangrove forest. Cells were curved rods and motile by means of a polar flagellum. Phylogenetic analysis based on 16S rRNA gene sequences showed that strain B20-1T belonged to the genus Marinomonas , sharing highest sequence similarities with Marinomonas rhizomae IVIA-Po-145T (97.6 %), Marinomonas dokdonensis DSW10-10T (97.0 %) and Marinomonas foliarum IVIA-Po-155T (96.9 %). The predominant cellular fatty acids of strain B20-1T were C10 : 0 3-OH, C18 : 1ω7c, summed feature 3 (C16 : 1ω7c and/or iso-C15 : 0 2-OH) and C16 : 0. Phosphatidylethanolamine and phosphatidylglycerol were identified as the predominant phospholipids. The predominant ubiquinone was Q-8. The genomic DNA G+C content of strain B20-1T was 46.6 mol%. On the basis of phenotypic characteristics, phylogenetic analysis and DNA–DNA relatedness, a novel species, Marinomonas mangrovi sp. nov., is proposed with B20-1T ( = DSM 28136T = LMG 28077T) as the type strain.


2012 ◽  
Vol 62 (Pt_12) ◽  
pp. 2997-3002 ◽  
Author(s):  
Neha Niharika ◽  
Swati Jindal ◽  
Jasvinder Kaur ◽  
Rup Lal

A bacterial strain, designated Dd16T, was isolated from a hexachlorocyclohexane (HCH) dumpsite at Lucknow, India. Cells of strain Dd16T were Gram-stain-negative, non-motile, rod-shaped and yellow-pigmented. Phylogenetic analysis based on 16S rRNA gene sequences showed that the strain belonged to the genus Sphingomonas in the family Sphingomonadaceae , as it showed highest sequence similarity to Sphingomonas asaccharolytica IFO 15499T (95.36 %), Sphingosinicella vermicomposti YC7378T (95.30), ‘Sphingomonas humi’ PB323 (95.20 %), Sphingomonas sanxanigenens NX02T (95.14 %) and Sphingomonas desiccabilis CP1DT (95.00 %). The major fatty acids were summed feature 3 (C16 : 1ω7c/C16 : 1ω6c) C14 : 0 2-OH, summed feature 8 (C18 : 1ω7c and/or C18 : 1ω6c) and C16 : 0. The polar lipid profile of strain Dd16T also corresponded to those reported for species of the genus Sphingomonas (phosphatidylethanolamine, diphosphatidylglycerol, phosphatidylcholine, phosphatidylglycerol, and a sphingoglycolipid), again supporting its identification as a member of the genus Sphingomonas . The predominant respiratory quinone was ubiquinone Q10, and sym-homospermidine was the major polyamine observed. The total DNA G+C content of strain Dd16T was 65.8 mol%. The results obtained on the basis of phenotypic characteristics and phylogenetic analysis and after biochemical and physiological tests, clearly distinguished strain Dd16T from closely related members of the genus Sphingomonas . Thus, strain Dd16T represents a novel species of the genus Sphingomonas for which the name Sphingomonas indica sp. nov. is proposed. The type strain is Dd16T ( = DSM 25434T = CCM 7882T).


Parasitology ◽  
2019 ◽  
Vol 146 (9) ◽  
pp. 1109-1115 ◽  
Author(s):  
Robert P. Hirt

AbstractMicrobial parasites adapted to thrive at mammalian mucosal surfaces have evolved multiple times from phylogenetically distant lineages into various extracellular and intracellular life styles. Their symbiotic relationships can range from commensalism to parasitism and more recently some host–parasites interactions are thought to have evolved into mutualistic associations too. It is increasingly appreciated that this diversity of symbiotic outcomes is the product of a complex network of parasites–microbiota–host interactions. Refinement and broader use of DNA based detection techniques are providing increasing evidence of how common some mucosal microbial parasites are and their host range, with some species being able to swap hosts, including from farm and pet animals to humans. A selection of examples will illustrate the zoonotic potential for a number of microbial parasites and how some species can be either disruptive or beneficial nodes in the complex networks of host–microbe interactions disrupting or maintaining mucosal homoeostasis. It will be argued that mucosal microbial parasitic diversity will represent an important resource to help us dissect through comparative studies the role of host–microbe interactions in both human health and disease.


mBio ◽  
2019 ◽  
Vol 10 (6) ◽  
Author(s):  
Tjorven Hinzke ◽  
Manuel Kleiner ◽  
Corinna Breusing ◽  
Horst Felbeck ◽  
Robert Häsler ◽  
...  

ABSTRACT The deep-sea tubeworm Riftia pachyptila lacks a digestive system but completely relies on bacterial endosymbionts for nutrition. Although the symbiont has been studied in detail on the molecular level, such analyses were unavailable for the animal host, because sequence information was lacking. To identify host-symbiont interaction mechanisms, we therefore sequenced the Riftia transcriptome, which served as a basis for comparative metaproteomic analyses of symbiont-containing versus symbiont-free tissues, both under energy-rich and energy-limited conditions. Our results suggest that metabolic interactions include nutrient allocation from symbiont to host by symbiont digestion and substrate transfer to the symbiont by abundant host proteins. We furthermore propose that Riftia maintains its symbiont by protecting the bacteria from oxidative damage while also exerting symbiont population control. Eukaryote-like symbiont proteins might facilitate intracellular symbiont persistence. Energy limitation apparently leads to reduced symbiont biomass and increased symbiont digestion. Our study provides unprecedented insights into host-microbe interactions that shape this highly efficient symbiosis. IMPORTANCE All animals are associated with microorganisms; hence, host-microbe interactions are of fundamental importance for life on earth. However, we know little about the molecular basis of these interactions. Therefore, we studied the deep-sea Riftia pachyptila symbiosis, a model association in which the tubeworm host is associated with only one phylotype of endosymbiotic bacteria and completely depends on this sulfur-oxidizing symbiont for nutrition. Using a metaproteomics approach, we identified both metabolic interaction processes, such as substrate transfer between the two partners, and interactions that serve to maintain the symbiotic balance, e.g., host efforts to control the symbiont population or symbiont strategies to modulate these host efforts. We suggest that these interactions are essential principles of mutualistic animal-microbe associations.


2020 ◽  
Vol 94 (10) ◽  
Author(s):  
Ling Chen ◽  
Quan Liu ◽  
Jiqiang Fan ◽  
Tingwei Yan ◽  
Haoran Zhang ◽  
...  

ABSTRACT A novel lytic bacteriophage, ValSw3-3, which efficiently infects pathogenic strains of Vibrio alginolyticus, was isolated from sewage water and characterized by microbiological and in silico genomic analyses. Transmission electron microscopy indicated that ValSw3-3 has the morphology of siphoviruses. This phage can infect four species in the Vibrio genus and has a latent period of 15 min and a burst size of 95 ± 2 PFU/infected bacterium. Genome sequencing results show that ValSw3-3 has a 39,846-bp double-stranded DNA genome with a GC content of 43.1%. The similarity between the genome sequences of ValSw3-3 and those of other phages recorded in the GenBank database was below 50% (42%), suggesting that ValSw3-3 significantly differs from previously reported phages at the DNA level. Multiple genome comparisons and phylogenetic analysis based on the major capsid protein revealed that phage ValSw3-3 is grouped in a clade with five other phages, including Listonella phage phiHSIC (GenBank accession no. NC_006953.1), Vibrio phage P23 (MK097141.1), Vibrio phage pYD8-B (NC_021561.1), Vibrio phage 2E1 (KX507045.1), and Vibrio phage 12G5 (HQ632860.1), and is distinct from all known genera within the Siphoviridae family that have been ratified by the International Committee on Taxonomy of Viruses (ICTV). An in silico proteomic comparison of diverse phages from the Siphoviridae family supported this clustering result and suggested that ValSw3-3, phiHSIC, P23, pYD8-B, 2E1, and 12G5 should be classified as a novel genus cluster of Siphoviridae. A subsequent analysis of core genes also revealed the common genes shared within this new cluster. Overall, these results provide a characterization of Vibrio phage ValSw3-3 and support our proposal of a new viral genus within the family Siphoviridae. IMPORTANCE Phage therapy has been considered a potential alternative to antibiotic therapy in treating bacterial infections. For controlling the vibriosis-causing pathogen Vibrio alginolyticus, well-documented phage candidates are still lacking. Here, we characterize a novel lytic Vibrio phage, ValSw3-3, based on its morphology, host range and infectivity, growth characteristics, stability under various conditions, and genomic features. Our results show that ValSw3-3 could be a potent candidate for phage therapy to treat V. alginolyticus infections due to its stronger infectivity and better pH and thermal stability than those of previously reported Vibrio phages. Moreover, genome sequence alignments, phylogenetic analysis, in silico proteomic comparison, and core gene analysis all support that this novel phage, ValSw3-3, and five unclassified phages form a clade distant from those of other known genera ratified by the ICTV. Thus, we propose a new viral genus within the Siphoviridae family to accommodate this clade, with ValSw3-3 as a representative member.


2014 ◽  
Vol 64 (Pt_2) ◽  
pp. 638-641 ◽  
Author(s):  
Liguang Zhou ◽  
Xiaoli Liu ◽  
Xiuzhu Dong

A psychrotolerant methanogenic strain, X-18T, was isolated from the soil of the Madoi wetland at Qinghai, Tibetan plateau, China. Cells were wavy rods (11–62 µm long) with blunt tapered ends and Gram-stain-negative. Strain X-18T grew strictly anaerobically and produced methane exclusively from H2/CO2. Growth occurred in the temperature range of 4–32 °C and optimally at 25 °C. Growth pH ranged from 6.5 to 8.0 and the optimum was 7.0. The G+C content of the genomic DNA of strain X-18T was 44.4 mol%. Phylogenetic analysis based on 16S rRNA gene sequences and the alpha subunit of methyl-coenzyme M reductase indicated that strain X-18T was affiliated to the genus Methanospirillum and was most closely related to Methanospirillum lacunae Ki8-1T, with 96.3 % 16S rRNA gene sequence similarity. However, strain X-18T could be distinguished from the existing species of the genus Methanospirillum by its lower growth temperature and obligate hydrogenotrophic methanogenesis. On the basis of phenotypic characteristics and phylogenetic analysis, strain X-18T represents a novel species of the genus Methanospirillum , for which the name Methanospirillum psychrodurum sp. nov. is proposed and strain X-18T is assigned as the type strain ( = CGMCC 1.5186T = JCM 19216T).


2013 ◽  
Vol 63 (Pt_3) ◽  
pp. 1132-1137 ◽  
Author(s):  
Li-Na Sun ◽  
Jun Zhang ◽  
Soon-Wo Kwon ◽  
Jian He ◽  
Shun-Gui Zhou ◽  
...  

A facultatively anaerobic, non-spore-forming, non-motile, catalase- and oxidase-positive, Gram-reaction-negative, coccoid to short rod-shaped strain, designated FLN-7T, was isolated from activated sludge of a wastewater biotreatment facility. The strain was able to hydrolyse amide pesticides (e.g. diflubenzuron, propanil, chlorpropham and dimethoate) through amide bond cleavage. Strain FLN-7T grew at 4–42 °C (optimum 28 °C), at pH 5.0–8.0 (optimum pH 7.0) and with 0–5.0 % (w/v) NaCl (optimum 1.0 %). The major respiratory quinone was ubiquinone-10. The major cellular fatty acid was C18 : 1ω7c. The genomic DNA G+C content of strain FLN-7T was 66.4±0.5 mol%. The major polar lipids were phosphatidylglycerol, phosphatidylethanolamine, diphosphatidylglycerol, phosphatidylcholine and an unidentified glycolipid. Phylogenetic analysis based on 16S rRNA gene sequences revealed that strain FLN-7T was a member of the genus Paracoccus and showed highest 16S rRNA gene sequence similarities with Paracoccus aminovorans JCM 7685T (99.2 %), P. denitrificans DSM 413T (97.8 %), P. yeei CDC G1212T (97.3 %) and P. thiocyanatus THI 011T (97.1 %). Strain FLN-7T showed low DNA–DNA relatedness with P. aminovorans KACC 12261T (36.5±3.4 %), P. denitrificans KACC 12251T (30.5±2.6 %), P. yeei CCUG 46822T (26.2±2.4 %) and P. thiocyanatus KACC 13901T (15.5±0.9 %). Based on the phylogenetic analysis, DNA–DNA hybridization, whole-cell fatty acid composition and biochemical characteristics, strain FLN-7T was clearly distinguished from all recognized species of the genus Paracoccus and should be classified in a novel species, for which the name Paracoccus huijuniae sp. nov. is proposed. The type strain is FLN-7T ( = KACC 16242T  = ACCC 05690T).


Sign in / Sign up

Export Citation Format

Share Document