TonB systems are required for Aeromonas hydrophila motility by controlling the secretion of flagellin

Dong, Yuhao; Xu, Meng; Wan, Xihe; Zhao, Dan; Geng, Jinzhu; Huang, Hao; Jiang, Mingguo; Chen, Lu; Liu, Yongjie

doi:10.1016/j.micinf.2022.105038

“…The TonB system was originally found and has been extensively characterized in E. coli (Postle and Larsen, 2007). E. coli and many other bacteria carry a single set of the TonB system, but after finding two TonB systems in V. cholerae (Occhino et al, 1998), multiple TonB systems have been identified and characterized in a number of bacteria, including many Vibrio species (2 or 3 systems) (Seliger et al, 2001;Stork et al, 2004;Alice et al, 2008;Wang et al, 2008;Tanabe et al, 2012), Aeromonas hydrophila (3 systems) (Dong et al, 2016;Dong et al, 2019;Dong et al, 2023), Pseudomonas aeruginosa (3 systems) (Poole et al, 1996;Zhao and Poole, 2000;Huang et al, 2004), Acinetobacter baumannii (3 systems) (Zimbler et al, 2013;Runci et al, 2019), and Bacteroides fragilis (6 systems) (Parker et al, 2022). In those examples, some TonB systems are functionally independent while others show functionally redundancy, for transport for particular substances such as siderophores and other nutrients, or physiological activities.…”

Section: Discussionmentioning

confidence: 99%

The dual role of TonB genes in turnerbactin uptake and carbohydrate utilization in the shipworm symbiontTeredinibacter turnerae

Naka

¹

,

Haygood

²

2023

Preprint

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Teredinibacter turneraeis an intracellular bacterial symbiont that resides in the gills of shipworms, wood-eating bivalve mollusks. This bacterium produces a catechol siderophore, turnerbactin, required for the survival of this bacterium under iron limiting conditions. The turnerbactin biosynthetic genes are contained in one of the secondary metabolite clusters conserved amongT. turneraestrains. However, Fe(III)-turnerbactin uptake mechanisms are largely unknown. Here, we show that the first gene of the cluster,fttAa homologue of Fe(III)-siderophore TonB-dependent outer membrane receptor (TBDR) genes is indispensable for iron uptake via the endogenous siderophore, turnerbactin, as well as by an exogenous siderophore, amphi-enterobactin, ubiquitously produced by marine vibrios. Furthermore, three TonB clusters containing fourtonBgenes were identified, and two of these genes,tonB1bandtonB2, functioned not only for iron transport but also for carbohydrate utilization when cellulose was a sole carbon source. Gene expression analysis revealed that none of thetonBgenes and other genes in those clusters were clearly regulated by iron concentration while turnerbactin biosynthesis and uptake genes were up-regulated under iron limiting conditions, highlighting the importance oftonBgenes even in iron rich conditions, possibly for utilization of carbohydrates derived from cellulose.

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“…The TonB system was originally found and has been extensively characterized in E. coli ( 65 ). E. coli and many other bacteria carry a single set of the TonB system, but after finding two TonB systems in V. cholerae ( 50 ), multiple TonB systems have been identified and characterized in a number of bacteria, including many Vibrio species (two or three systems) ( 51 , 52 , 66 – 68 ), Aeromonas hydrophila (three systems) ( 69 – 71 ), Pseudomonas aeruginosa (three systems) ( 63 , 72 , 73 ), Acinetobacter baumannii (three systems) ( 74 , 75 ), and Bacteroides fragilis (six systems) ( 76 ). In those examples, some TonB systems are functionally independent while others show functional redundancy, for transport for particular substances such as siderophores and other nutrients, or physiological activities.…”

Section: Discussionmentioning

confidence: 99%

The dual role of TonB genes in turnerbactin uptake and carbohydrate utilization in the shipworm symbiont Teredinibacter turnerae

Naka,

Haygood

2023

Appl Environ Microbiol

0

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Teredinibacter turnerae is an intracellular bacterial symbiont that resides in the gills of shipworms, wood-eating bivalve mollusks. This bacterium produces a catechol siderophore, turnerbactin, required for the survival of this bacterium under iron-limiting conditions. The turnerbactin biosynthetic genes are contained in one of the secondary metabolite clusters conserved among T. turnerae strains. However, Fe(III)-turnerbactin uptake mechanisms are largely unknown. Here, we show that the first gene of the cluster, fttA , a homolog of Fe(III)-siderophore TonB-dependent outer membrane receptor genes, is indispensable for iron uptake via the endogenous siderophore, turnerbactin, as well as by an exogenous siderophore, amphi-enterobactin, ubiquitously produced by marine vibrios. Furthermore, three TonB clusters containing four tonB genes were identified, and two of these genes, tonB1b and tonB2 , functioned not only for iron transport but also for carbohydrate utilization when cellulose was a sole carbon source. Gene expression analysis revealed that none of the tonB genes and other genes in those clusters were clearly regulated by iron concentration while turnerbactin biosynthesis and uptake genes were upregulated under iron-limiting conditions, highlighting the importance of tonB genes even in iron-rich conditions, possibly for utilization of carbohydrates derived from cellulose. IMPORTANCE This study highlights diversity in iron acquisition and regulation in bacteria. The mechanisms of iron acquisition and its regulation in Teredinibacter turnerae , as well as its connection to cellulose utilization, a hallmark phenotype of T. turnerae , expand the paradigm of bacterial iron acquisition. Two of the four TonB genes identified in T. turnerae exhibit functional redundancy and play a crucial role in siderophore-mediated iron transport. Unlike typical TonB genes in bacteria, none of the TonB genes in T. turnerae are clearly iron regulated. This unusual regulation could be explained by another important finding in this study, namely, that the two TonB genes involved in iron transport are also essential for cellulose utilization as a carbon source, leading to the expression of TonB genes even under iron-rich conditions.

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Aeromonas hydrophila infection in acute myeloid leukemia: A case report

He,

Zhong,

Fan

2023

Asian Pacific Journal of Tropical Medicine

1

0

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Rationale: Aeromonas hydrophila, a bacterium commonly found in a variety of soils, aquatic habitats, and other natural environments, is known for causing infections and hemorrhagic diseases in both aquatic and terrestrial animals. Patients with leukemia, when infected by Aeromonas hydrophila following chemotherapy, face an increased risk of developing necrotizing fasciitis. Patient concerns: A 48-year-old male with a history of acute myeloid leukemia presented with swelling and pain in his right hand after being stabbed by a grass carp two days ago. The injury occurred on the fifth day after his last chemotherapy session when he was accidentally punctured in the right thumb and ring finger by a carp while fishing. Two days following the injury, the skin isurrounding the wound turned black immediately, while the rest of his hand was reddened, swollen, and bleeding. Diagnosis: Aeromonas hydrophila infection in the soft tissue of the right hand. Interventions: Intravenous antibiotics and local debridement. Outcomes: The patient experienced an alleviation of systemic poisoning symptoms, effective control of the local wound infection. Lessons: It is important for physicians to appreciate the potential for highly unusual and life-threatening infections in patients with acute myeloid leukemia. Early diagnosis and prompt treatment can prevent the development of necrotizing fasciitis and save patients' lives.

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TonB systems are required for Aeromonas hydrophila motility by controlling the secretion of flagellin

Cited by 3 publications

References 37 publications

The dual role of TonB genes in turnerbactin uptake and carbohydrate utilization in the shipworm symbiontTeredinibacter turnerae

The dual role of TonB genes in turnerbactin uptake and carbohydrate utilization in the shipworm symbiontTeredinibacter turnerae

The dual role of TonB genes in turnerbactin uptake and carbohydrate utilization in the shipworm symbiont Teredinibacter turnerae

Aeromonas hydrophila infection in acute myeloid leukemia: A case report

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