Literature DB >> 28159791

Microaerophilic Fe(II)-Oxidizing Zetaproteobacteria Isolated from Low-Fe Marine Coastal Sediments: Physiology and Composition of Their Twisted Stalks.

K Laufer1, M Nordhoff1, M Halama1, R E Martinez2, M Obst3, M Nowak4, H Stryhanyuk5, H H Richnow5, A Kappler6,7.   

Abstract

Microaerophilic Fe(II) oxidizers are commonly found in habitats containing elevated Fe(II) and low O2 concentrations and often produce characteristic Fe mineral structures, so-called twisted stalks or tubular sheaths. Isolates originating from freshwater habitats are all members of the Betaproteobacteria, while isolates from marine habitats belong almost exclusively to the Zetaproteobacteria So far, only a few isolates of marine microaerophilic Fe(II) oxidizers have been described, all of which are obligate microaerophilic Fe(II) oxidizers and have been thought to be restricted to Fe-rich systems. Here, we present two new isolates of marine microaerophilic Fe(II)-oxidizing Zetaproteobacteria that originate from typical coastal marine sediments containing only low Fe concentrations (2 to 11 mg of total Fe/g of sediment [dry weight]; 70 to 100 μM dissolved Fe2+ in the porewater). The two novel Zetaproteobacteria share characteristic physiological properties of the Zetaproteobacteria group, even though they come from low-Fe environments: the isolates are obligate microaerophilic Fe(II) oxidizers and, like most isolated Zetaproteobacteria, they produce twisted stalks. We found a low organic carbon content in the stalks (∼0.3 wt%), with mostly polysaccharides and saturated aliphatic chains (most likely lipids). The Fe minerals in the stalks were identified as lepidocrocite and possibly ferrihydrite. Immobilization experiments with Ni2+ showed that the stalks can function as a sink for trace metals. Our findings show that obligate microaerophilic Fe(II) oxidizers belonging to the Zetaproteobacteria group are not restricted to Fe-rich environments but can also be found in low-Fe marine environments, which increases their overall importance for the global biogeochemical Fe cycle.IMPORTANCE So far, only a few isolates of benthic marine microaerophilic Fe(II) oxidizers belonging to the Zetaproteobacteria exist, and most isolates were obtained from habitats containing elevated Fe concentrations. Consequently, it was thought that these microorganisms are important mainly in habitats with high Fe concentrations. The two novel isolates of Zetaproteobacteria that are presented in the present study were isolated from typical coastal marine sediments that do not contain elevated Fe concentrations. This increases the knowledge about possible habitats in which Zetaproteobacteria can exist. Furthermore, we show that the physiology and the typical organo-mineral structures (twisted stalks) that are produced by the isolates do not notably differ from the physiology and the cell-mineral structures of isolates from environments with high Fe concentrations. We also showed that the organo-mineral structures can function as a sink for trace metals.
Copyright © 2017 American Society for Microbiology.

Entities:  

Keywords:  geomicrobiology; iron oxidizers; marine microbiology; sediment

Mesh:

Substances:

Year:  2017        PMID: 28159791      PMCID: PMC5377495          DOI: 10.1128/AEM.03118-16

Source DB:  PubMed          Journal:  Appl Environ Microbiol        ISSN: 0099-2240            Impact factor:   4.792


  64 in total

1.  Microbial communities in iron-silica-rich microbial mats at deep-sea hydrothermal fields of the Southern Mariana Trough.

Authors:  Shingo Kato; Chiyori Kobayashi; Takeshi Kakegawa; Akihiko Yamagishi
Journal:  Environ Microbiol       Date:  2009-04-22       Impact factor: 5.491

2.  The gill chamber epibiosis of deep-sea shrimp Rimicaris exoculata: an in-depth metagenomic investigation and discovery of Zetaproteobacteria.

Authors:  Cyrielle Jan; Jillian M Petersen; Johannes Werner; Hanno Teeling; Sixing Huang; Frank Oliver Glöckner; Olga V Golyshina; Nicole Dubilier; Peter N Golyshin; Mohamed Jebbar; Marie-Anne Cambon-Bonavita
Journal:  Environ Microbiol       Date:  2014-03-04       Impact factor: 5.491

3.  Neutrophilic Fe-oxidizing bacteria are abundant at the Loihi Seamount hydrothermal vents and play a major role in Fe oxide deposition.

Authors:  David Emerson; Craig L Moyer
Journal:  Appl Environ Microbiol       Date:  2002-06       Impact factor: 4.792

4.  Biodiversity and emerging biogeography of the neutrophilic iron-oxidizing Zetaproteobacteria.

Authors:  Sean M McAllister; Richard E Davis; Joyce M McBeth; Bradley M Tebo; David Emerson; Craig L Moyer
Journal:  Appl Environ Microbiol       Date:  2011-06-10       Impact factor: 4.792

5.  Nanometer-scale visualization and structural analysis of the inorganic/organic hybrid structure of Gallionella ferruginea twisted stalks.

Authors:  Tomoko Suzuki; Hideki Hashimoto; Nobuyuki Matsumoto; Mitsuaki Furutani; Hitoshi Kunoh; Jun Takada
Journal:  Appl Environ Microbiol       Date:  2011-03-04       Impact factor: 4.792

Review 6.  Iron-oxidizing bacteria: an environmental and genomic perspective.

Authors:  David Emerson; Emily J Fleming; Joyce M McBeth
Journal:  Annu Rev Microbiol       Date:  2010       Impact factor: 15.500

7.  Lithotrophic iron-oxidizing bacteria produce organic stalks to control mineral growth: implications for biosignature formation.

Authors:  Clara S Chan; Sirine C Fakra; David Emerson; Emily J Fleming; Katrina J Edwards
Journal:  ISME J       Date:  2010-11-25       Impact factor: 10.302

8.  Isolation and characterization of novel psychrophilic, neutrophilic, Fe-oxidizing, chemolithoautotrophic alpha- and gamma-proteobacteria from the deep sea.

Authors:  K J Edwards; D R Rogers; C O Wirsen; T M McCollom
Journal:  Appl Environ Microbiol       Date:  2003-05       Impact factor: 4.792

9.  Ultra-diffuse hydrothermal venting supports Fe-oxidizing bacteria and massive umber deposition at 5000 m off Hawaii.

Authors:  Katrina J Edwards; B T Glazer; O J Rouxel; W Bach; D Emerson; R E Davis; B M Toner; C S Chan; B M Tebo; H Staudigel; C L Moyer
Journal:  ISME J       Date:  2011-05-05       Impact factor: 10.302

10.  Ecophysiology of Zetaproteobacteria Associated with Shallow Hydrothermal Iron-Oxyhydroxide Deposits in Nagahama Bay of Satsuma Iwo-Jima, Japan.

Authors:  Tatsuhiko Hoshino; Takashi Kuratomi; Yuki Morono; Tomoyuki Hori; Hisashi Oiwane; Shoichi Kiyokawa; Fumio Inagaki
Journal:  Front Microbiol       Date:  2016-01-11       Impact factor: 5.640

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  10 in total

Review 1.  An evolving view on biogeochemical cycling of iron.

Authors:  Andreas Kappler; Casey Bryce; Muammar Mansor; Ulf Lueder; James M Byrne; Elizabeth D Swanner
Journal:  Nat Rev Microbiol       Date:  2021-02-01       Impact factor: 60.633

2.  Genomic Insights into Two Novel Fe(II)-Oxidizing Zetaproteobacteria Isolates Reveal Lifestyle Adaption to Coastal Marine Sediments.

Authors:  Nia Blackwell; Casey Bryce; Daniel Straub; Andreas Kappler; Sara Kleindienst
Journal:  Appl Environ Microbiol       Date:  2020-08-18       Impact factor: 4.792

Review 3.  Iron-oxidizing bacteria in marine environments: recent progresses and future directions.

Authors:  Hiroko Makita
Journal:  World J Microbiol Biotechnol       Date:  2018-07-04       Impact factor: 3.312

4.  Salinity Impact on Composition and Activity of Nitrate-Reducing Fe(II)-Oxidizing Microorganisms in Saline Lakes.

Authors:  Jianrong Huang; Mingxian Han; Jian Yang; Andreas Kappler; Hongchen Jiang
Journal:  Appl Environ Microbiol       Date:  2022-05-02       Impact factor: 5.005

5.  Aerobic and anaerobic iron oxidizers together drive denitrification and carbon cycling at marine iron-rich hydrothermal vents.

Authors:  Sean M McAllister; Rebecca Vandzura; Jessica L Keffer; Shawn W Polson; Clara S Chan
Journal:  ISME J       Date:  2020-12-17       Impact factor: 10.302

6.  Genomic expansion of magnetotactic bacteria reveals an early common origin of magnetotaxis with lineage-specific evolution.

Authors:  Wei Lin; Wensi Zhang; Xiang Zhao; Andrew P Roberts; Greig A Paterson; Dennis A Bazylinski; Yongxin Pan
Journal:  ISME J       Date:  2018-03-26       Impact factor: 10.302

Review 7.  The Fe(II)-oxidizing Zetaproteobacteria: historical, ecological and genomic perspectives.

Authors:  Sean M McAllister; Ryan M Moore; Amy Gartman; George W Luther; David Emerson; Clara S Chan
Journal:  FEMS Microbiol Ecol       Date:  2019-04-01       Impact factor: 4.194

8.  Validating the Cyc2 Neutrophilic Iron Oxidation Pathway Using Meta-omics of Zetaproteobacteria Iron Mats at Marine Hydrothermal Vents.

Authors:  Sean M McAllister; Shawn W Polson; David A Butterfield; Brian T Glazer; Jason B Sylvan; Clara S Chan
Journal:  mSystems       Date:  2020-02-18       Impact factor: 6.496

9.  Zetaproteobacteria Pan-Genome Reveals Candidate Gene Cluster for Twisted Stalk Biosynthesis and Export.

Authors:  Elif Koeksoy; Oliver M Bezuidt; Timm Bayer; Clara S Chan; David Emerson
Journal:  Front Microbiol       Date:  2021-06-18       Impact factor: 5.640

10.  Novel Pelagic Iron-Oxidizing Zetaproteobacteria from the Chesapeake Bay Oxic-Anoxic Transition Zone.

Authors:  Beverly K Chiu; Shingo Kato; Sean M McAllister; Erin K Field; Clara S Chan
Journal:  Front Microbiol       Date:  2017-07-18       Impact factor: 5.640

  10 in total

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