Microbial metalloproteomes are largely uncharacterized

Cvetkovic, Aleksandar; Menon, Angeli Lal; Thorgersen, Michael P.; Scott, Joseph W.; Poole, Farris L.; Jenney, Francis E.; Lancaster, W. Andrew; Praissman, Jeremy L.; Shanmukh, Saratchandra; Vaccaro, Brian J.; Trauger, Sunia A.; Kalisiak, Ewa; Apon, Junefredo V.; Siuzdak, Gary; Yannone, Steven M.; Tainer, John A.; Adams, Michael W. W.

doi:10.1038/nature09265

Cited by 321 publications

(305 citation statements)

References 32 publications

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“…These atmospheric inputs provide a variety of nutrients and trace metals (Table S1 and reviewed in Guieu et al, 2014), which are required for microbial cellular metabolism, enzymatic activity and growth (e.g., Cvetkovic et al, 2010;Huertas et al, 2014). In addition to nutrients and trace metals, atmospheric deposition may also introduce a wide array of airborne microorganisms to surface seawater (reviewed in Griffin, 2007;Polymenakou, 2012).…”

Section: Discussionmentioning

confidence: 99%

The Impact of Atmospheric Dry Deposition Associated Microbes on the Southeastern Mediterranean Sea Surface Water following an Intense Dust Storm

et al. 2016

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This study explores the potential impacts of microbes deposited into the surface seawater of the southeastern Mediterranean Sea (SEMS) along with atmospheric particles on marine autotrophic and heterotrophic production. We compared in situ changes in autotrophic and heterotrophic microbial abundance and production rates before and during an intense dust storm event in early September 2015. Additionally, we measured the activity of microbes associated with atmospheric dry deposition (also referred to as airborne microbes) in sterile SEMS water using the same particles collected during the dust storm. A high diversity of prokaryotes and a low diversity of autotrophic eukaryotic algae were delivered to surface SEMS waters by the storm. Autotrophic airborne microbial abundance and activity were low, contributing ∼1% of natural abundance in SEMS water and accounting for 1-4% to primary production. Airborne heterotrophic bacteria comprised 30-50% of the cells and accounted for 13-42% of bacterial production. Our results demonstrate that atmospheric dry deposition may supply not only chemical constitutes but also microbes that can affect ambient microbial populations and their activity in the surface ocean. Airborne microbes may play a greater role in ocean biogeochemistry in the future in light of the expected enhancement of dust storm durations and frequencies due to climate change and desertification processes.

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Section: Discussionmentioning

confidence: 99%

The Impact of Atmospheric Dry Deposition Associated Microbes on the Southeastern Mediterranean Sea Surface Water following an Intense Dust Storm

et al. 2016

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“…Although our knowledge of metaldependent proteins in bacteria is incomplete (22), nickel is a critical part of the catalytic center for at least two E. coli nickel-dependent enzymes identified to date (23).…”

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confidence: 99%

Uropathogenic enterobacteria use the yersiniabactin metallophore system to acquire nickel

Robinson¹,

Lowe²,

Koh³

et al. 2018

Journal of Biological Chemistry

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Invasive gram-negative bacteria often express multiple virulence-associated metal ion chelators to combat host-mediated metal deficiencies. Escherichia coli, Klebsiella, and Yersinia pestis isolates encoding the Yersinia High Pathogenicity Island (HPI) secrete yersiniabactin (Ybt), a metallophore originally shown to chelate iron ions during infection. However, our recent demonstration that Ybt also scavenges copper ions during infection led us to question whether it might be capable of retrieving other metals as well. Here, we find that uropathogenic E. coli also use Ybt to bind extracellular nickel ions. Using quantitative mass spectrometry, we show that the canonical metal-Ybt import pathway internalizes the resulting Ni-Ybt complexes, extracts the nickel, and releases metal-free Ybt back to the extracellular space. We find that E. coli and Klebsiella direct the nickel liberated from this pathway to intracellular nickel enzymes. Thus, Ybt may provide access to nickel that is inaccessible to the conserved NikABCDE permease system. Nickel should be considered alongside iron and copper as a plausible substrate for Ybt-mediated metal import by enterobacteria during human infections.E. coli and related enterobacteria are the predominant cause of human urinary tract infections (UTIs) and contribute substantially to the worldwide rise in antibiotic-resistant infections (1). Clinical enterobacterial isolates often possess additional, non-essential, virulenceassociated genes. Prominent among these is the Yersinia high pathogenicity island (HPI), which encodes the biosynthetic machinery to make the specialized metabolites yersiniabactin (Ybt) and escherichelin (2). Direct mass spectrometric detection of urinary Ybt in UTI patients, serological markers, transcriptional signatures, and experimental infection models all indicate active expression of Yersinia HPI proteins during UTI pathogenesis (3-7).Although initially understood as a siderophore-a chelator that binds Fe(III) for bacterial use-Ybt has recently been appreciated to exhibit a broader metal ion binding repertoire. Copper-Ybt complexes were observed in E. coli UTI patients and were connected to protection of E. coli from copper toxicity (7), an example of biological metal passivation. Because copper is an important nutrient, complete sequestration of copper ions by Ybt could starve uropathogenic E. coli (UPEC) of copper. However, UPEC retain nutritional access to Ybt-bound copper and iron by importing the metal-Ybt complexes in a controlled manner, extracting the metal, and using it to support metal-dependent cellular functions (8). These findings implicate Ybt as an agent of nutritional passivation, a biological strategy in which metal ion toxicity is minimized Ybt-mediated nickel acquisition 2 while nutritional access is preserved. In this manner, Ybt acts as an extracellular metal ion sink, with subsequent entry into the cell occurring as a controlled process. Whether this nutritional passivation activity of Ybt extends to biological metal ions beyon...

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“…Although some metalloenzymes have been characterized, the majority still remain uncharacterized or unknown 6 . One of the major challenges in measuring metalloproteins is the requirement to maintain the native state of the protein 7 .…”

Section: Introductionmentioning

confidence: 99%

Standards for Quantitative Metalloproteomic Analysis Using Size Exclusion ICP-MS

Lothian

Roberts

2016

JoVE

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Metals are essential for protein function as cofactors to catalyze chemical reactions. Disruption of metal homeostasis is implicated in a number of diseases including Alzheimer's and Parkinson's disease, but the exact role these metals play is yet to be fully elucidated. Identification of metalloproteins encounters many challenges and difficulties. Here we report an approach that allows metalloproteins in complex samples to be quantified. This is achieved using size exclusion chromatography coupled with inductively coupled plasma -mass spectrometry (SEC-ICP-MS). Using six known metalloproteins, the size exclusion column can be calibrated and the respective trace elements (iron, copper, zinc, cobalt, iodine) can be used for quantification. SEC-ICP-MS traces of human brain and plasma are presented. The use of these metalloprotein standards provides the means to quantitatively compare metalloprotein abundances between biological samples. This technique is poised to help shed light on the role of metalloproteins in neurodegenerative disease as well as other diseases where imbalances in trace elements are implicated.

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Microbial metalloproteomes are largely uncharacterized

Cited by 321 publications

References 32 publications

The Impact of Atmospheric Dry Deposition Associated Microbes on the Southeastern Mediterranean Sea Surface Water following an Intense Dust Storm

The Impact of Atmospheric Dry Deposition Associated Microbes on the Southeastern Mediterranean Sea Surface Water following an Intense Dust Storm

Uropathogenic enterobacteria use the yersiniabactin metallophore system to acquire nickel

Standards for Quantitative Metalloproteomic Analysis Using Size Exclusion ICP-MS

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