Proteomic response of the marine ammonia-oxidising archaeon Nitrosopumilus maritimus to iron limitation reveals strategies to compensate for nutrient scarcity.

Roxana T Shafiee,Svenja Hester,Rosalind E M Rickaby,Joseph T Snow,Qiong Zhang

doi:10.1111/1462-2920.15491

Roxana T Shafiee, Svenja Hester + Show 3 more

Open Access

https://doi.org/10.1111/1462-2920.15491

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Abstract

Dissolved iron (Fe) is vanishingly low in the oceans, with ecological success conferred to microorganisms that can restructure their biochemistry to maintain high growth rates during Fe scarcity. Chemolithoautotrophic ammonia-oxidising archaea (AOA) are highly abundant in the oceans, constituting ~30% of cells below the photic zone. Here we examine the proteomic response of the AOA isolate Nitrosopumilus maritimus to growth-limiting Fe concentrations. Under Fe limitation, we observed a significant reduction in the intensity of Fe-dense ferredoxins associated with respiratory complex I whilst complex III and IV proteins with more central roles in the electron transport chain remain unchanged. We concomitantly observed an increase in the intensity of Fe-free functional alternatives such as flavodoxin and plastocyanin, thioredoxin and alkyl hydroperoxide which are known to mediate electron transport and reactive oxygen species detoxification, respectively. Under Fe limitation, we found a marked increase in the intensity of the ABC phosphonate transport system (Phn), highlighting an intriguing link between Fe and P cycling in N. maritimus. We hypothesise that an elevated uptake of exogenous phosphonates under Fe limitation may either supplement N. maritimus' endogenous methylphosphonate biosynthesis pathway - which requires Fe - or enhance the production of phosphonate-containing exopolysaccharides known to efficiently bind environmental Fe.

Highlights

Ammonia-oxidising archaea (AOA) occupy a diverse array of ecosystems from hot springs to the oligotrophic open ocean
We demonstrated that the model AOA isolate Nitrosopumilus maritimus strain SCM1, despite possessing a unique Cu-dominated centric biochemistry compared to its ammonia-oxidising bacterial counterparts (Walker et al, 2010; Amin et al, 2013; Shafiee et al,2021), requires a greater concentration of unchelated Fe (Fe0) for growth than many cosmopolitan marine microorganisms (Shafiee et al, 2019)
We present the label-free quantitative intensity profiles of N. maritimus under Fe-limited and Fereplete growth, thereby gaining important insight into the potential mechanisms adopted by AOA to navigate Fe scarcity

Summary

Introduction

Ammonia-oxidising archaea (AOA) occupy a diverse array of ecosystems from hot springs to the oligotrophic open ocean. A greater Fe requirement for growth relative to other marine microorganisms suggests that AOA must occupy an Ferich niche and aligns with observations of AOA maxima at the base of the photic zone (Santoro et al, 2013; Shiozaki et al, 2016). At this depth, Fe supply is great due to the combined effect of a decrease in competition for Fe (as phytoplankton become light limited) and Fe remineralisation from sinking organic matter. The application of proteomic biomarkers provides a powerful alternative to traditional nutrient amendment experiments - which often alter community composition and do not necessarily capture the multicomplexed nature of stressors - which can be applied to wide geographic regions

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