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Description: The genus Nitrospira is the most widespread group of nitrite-oxidizing bacteria and thrives in diverse natural and engineered ecosystems. Nitrospira marina Nb-295T was isolated from the ocean over 30 years ago; however, its genome has not yet been analyzed. Here, we investigated the metabolic potential of N. marina based on its complete genome sequence and performed physiological experiments to test genome-derived hypotheses. Our data confirm that N. marina benefits from additions of undefined organic carbon substrates, has adaptations to resist oxidative, osmotic, and UV light-induced stress and low dissolved pCO2, and requires exogenous vitamin B12. In addition, N. marina is able to grow chemoorganotrophically on formate, and is thus not an obligate chemolithoautotroph. We further investigated the proteomic response of N. marina to low (∼5.6 µM) O2 concentrations. The abundance of a potentially more efficient CO2-fixing pyruvate:ferredoxin oxidoreductase (POR) complex and a high-affinity cbb3-type terminal oxidase increased under O2 limitation, suggesting a role in sustaining nitrite oxidation-driven autotrophy. This putatively more O2-sensitive POR complex might be protected from oxidative damage by Cu/Zn-binding superoxide dismutase, which also increased in abundance under low O2 conditions. Furthermore, the upregulation of proteins involved in alternative energy metabolisms, including Group 3b [NiFe] hydrogenase and formate dehydrogenase, indicate a high metabolic versatility to survive conditions unfavorable for aerobic nitrite oxidation. In summary, the genome and proteome of the first marine Nitrospira isolate identifies adaptations to life in the oxic ocean and provides insights into the metabolic diversity and niche differentiation of NOB in marine environments.

Print ISSN: 1751-7362

Electronic ISSN: 1751-7370

Topics: Biology

Published by Springer Nature

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Dissolved and particulate trace metal micronutrients under the McMurdo Sound seasonal sea ice : basal sea ice communities as a capacitor for iron (2014)

Noble, Abigail E. ; Moran, Dawn M. ; Allen, Andrew E. ; [et al.]

Frontiers Media

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Publication Date: 2022-05-26

Description: © The Author(s), 2013. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Chemistry 1 (2013): 25, doi:10.3389/fchem.2013.00025.

Description: Dissolved and particulate metal concentrations are reported from three sites beneath and at the base of the McMurdo Sound seasonal sea ice in the Ross Sea of Antarctica. This dataset provided insight into Co and Mn biogeochemistry, supporting a previous hypothesis for water column mixing occurring faster than scavenging. Three observations support this: first, Mn-containing particles with Mn/Al ratios in excess of the sediment were present in the water column, implying the presence of bacterial Mn-oxidation processes. Second, dissolved and labile Co were uniform with depth beneath the sea ice after the winter season. Third, dissolved Co:PO3−4 ratios were consistent with previously observed Ross Sea stoichiometry, implying that over-winter scavenging was slow relative to mixing. Abundant dissolved Fe and Mn were consistent with a winter reserve concept, and particulate Al, Fe, Mn, and Co covaried, implying that these metals behaved similarly. Elevated particulate metals were observed in proximity to the nearby Islands, with particulate Fe/Al ratios similar to that of nearby sediment, consistent with a sediment resuspension source. Dissolved and particulate metals were elevated at the shallowest depths (particularly Fe) with elevated particulate P/Al and Fe/Al ratios in excess of sediments, demonstrating a sea ice biomass source. The sea ice biomass was extremely dense (chl a 〉9500 μg/L) and contained high abundances of particulate metals with elevated metal/Al ratios. A hypothesis for seasonal accumulation of bioactive metals at the base of the McMurdo Sound sea ice by the basal algal community is presented, analogous to a capacitor that accumulates iron during the spring and early summer. The release and transport of particulate metals accumulated at the base of the sea ice by sloughing is discussed as a potentially important mechanism in providing iron nutrition during polynya phytoplankton bloom formation and could be examined in future oceanographic expeditions.

Description: This research was funded by NSF OPP grant 0732665, NSF-OCE grant numbers 1031271, 0928414, 0752291, 1233261, and the Gordon and Betty Moore Foundation.

Repository Name: Woods Hole Open Access Server

Type: Article

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Unique patterns and biogeochemical relevance of two-component sensing in marine bacteria. (2019)

Held, Noelle A. ; McIlvin, Matthew R. ; Moran, Dawn M. ; [et al.]

American Society for Microbiology Journals

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Publication Date: 2022-10-26

Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 License. The definitive version was published in mSystems 4(1), (2019): 4:e00317-18, doi:10.1128/mSystems.00317-18.

Description: Two-component sensory (TCS) systems link microbial physiology to the environment and thus may play key roles in biogeochemical cycles. In this study, we surveyed the TCS systems of 328 diverse marine bacterial species. We identified lifestyle traits such as copiotrophy and diazotrophy that are associated with larger numbers of TCS system genes within the genome. We compared marine bacterial species with 1,152 reference bacterial species from a variety of habitats and found evidence of extra response regulators in marine genomes. Examining the location of TCS genes along the circular bacterial genome, we also found that marine bacteria have a large number of “orphan” genes, as well as many hybrid histidine kinases. The prevalence of “extra” response regulators, orphan genes, and hybrid TCS systems suggests that marine bacteria break with traditional understanding of how TCS systems operate. These trends suggest prevalent regulatory networking, which may allow coordinated physiological responses to multiple environmental signals and may represent a specific adaptation to the marine environment. We examine phylogenetic and lifestyle traits that influence the number and structure of two-component systems in the genome, finding, for example, that a lack of two-component systems is a hallmark of oligotrophy. Finally, in an effort to demonstrate the importance of TCS systems to marine biogeochemistry, we examined the distribution of Prochlorococcus/Synechococcus response regulator PMT9312_0717 in metaproteomes of the tropical South Pacific. We found that this protein’s abundance is related to phosphate concentrations, consistent with a putative role in phosphate regulation.

Description: We thank Joe Jennings at Oregon State University and Chris Dupont at the J. Craig Venter Institute for providing nutrient and metagenomic analyses, respectively, for the KM1128 METZYME research expedition. We also thank our anonymous reviewers for their thoughtful comments. This material is based on work supported by a National Science Foundation Graduate Research Fellowship under grant number 1122274 (N. A. Held). It was also supported by the Gordon and Betty Moore Foundation (grant number 3782 [M. Saito]) and by the National Science Foundation (grant numbers OCE-1657766, EarthCube 1639714, OCE-1658030, and OCE-1260233).

Keywords: Biogeochemistry ; Cell signaling ; Gene regulation ; Marine microbiology ; Proteomics ; Regulatory network ; Two-component system

Repository Name: Woods Hole Open Access Server

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Examination of microbial proteome preservation techniques applicable to autonomous environmental sample collection (2014)

Saito, Mak A. ; Bulygin, Vladimir V. ; Moran, Dawn M. ; [et al.]

Frontiers Media

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Publication Date: 2022-05-26

Description: © The Author(s), 2011. This is an open-access article subject to a non-exclusive license between the authors and Frontiers Media SA, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited. The definitive version was published in Frontiers in Microbiology 2 (2011): 215, doi:10.3389/fmicb.2011.00215.

Description: Improvements in temporal and spatial sampling frequency have the potential to open new windows into the understanding of marine microbial dynamics. In recent years, efforts have been made to allow automated samplers to collect microbial biomass for DNA/RNA analyses from moored observatories and autonomous underwater vehicles. Measurements of microbial proteins are also of significant interest given their biogeochemical importance as enzymes that catalyze reactions and transporters that interface with the environment. We examined the influence of five preservatives solutions (SDS-extraction buffer, ethanol, trichloroacetic acid, B-PER, and RNAlater) on the proteome integrity of the marine cyanobacterium Synechococcus WH8102 after 4 weeks of storage at room temperature. Four approaches were used to assess degradation: total protein recovery, band integrity on an SDS detergent polyacrylamide electrophoresis (SDS-PAGE) gel, and number of protein identifications and relative abundances by 1-dimensional LC–MS/MS proteomic analyses. Total protein recoveries from the preserved samples were lower than the frozen control due to processing losses, which could be corrected for with internal standardization. The trichloroacetic acid preserved sample showed significant loss of protein band integrity on the SDS-PAGE gel. The RNAlater preserved sample showed the highest number of protein identifications (103% relative to the control; 520 ± 31 identifications in RNAlater versus 504 ± 4 in the control), equivalent to the frozen control. Relative abundances of individual proteins in the RNAlater treatment were quite similar to that of the frozen control (average ratio of 1.01 ± 0.27 for the 50 most abundant proteins), while the SDS-extraction buffer, ethanol, and B-PER all showed significant decreases in both number of identifications and relative abundances of individual proteins. Based on these findings, RNAlater was an effective proteome preservative, although further study is warranted on additional marine microbes.

Description: This work was funded by the National Science Foundation Chemical and Biological Oceanography, Center for Microbial Oceanography Research and Education (C-MORE), and the Gordon and Betty Moore Foundation.

Keywords: Proteome ; Preservation ; Autonomous sampling ; Cyanobacteria ; Alkaline phosphatase ; Proteomics ; Synechococcus WH8102

Repository Name: Woods Hole Open Access Server

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Metabolic versatility of the nitrite-oxidizing bacterium Nitrospira marina and its proteomic response to oxygen-limited conditions (2021)

Bayer, Barbara ; Saito, Mak A. ; McIlvin, Matthew R. ; [et al.]

Springer Nature

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Publication Date: 2022-05-26

Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Bayer, B., Saito, M. A., McIlvin, M. R., Lucker, S., Moran, D. M., Lankiewicz, T. S., Dupont, C. L., & Santoro, A. E. (2020). Metabolic versatility of the nitrite-oxidizing bacterium Nitrospira marina and its proteomic response to oxygen-limited conditions. Isme Journal, doi:10.1038/s41396-020-00828-3.

Description: The genus Nitrospira is the most widespread group of nitrite-oxidizing bacteria and thrives in diverse natural and engineered ecosystems. Nitrospira marina Nb-295T was isolated from the ocean over 30 years ago; however, its genome has not yet been analyzed. Here, we investigated the metabolic potential of N. marina based on its complete genome sequence and performed physiological experiments to test genome-derived hypotheses. Our data confirm that N. marina benefits from additions of undefined organic carbon substrates, has adaptations to resist oxidative, osmotic, and UV light-induced stress and low dissolved pCO2, and requires exogenous vitamin B12. In addition, N. marina is able to grow chemoorganotrophically on formate, and is thus not an obligate chemolithoautotroph. We further investigated the proteomic response of N. marina to low (∼5.6 µM) O2 concentrations. The abundance of a potentially more efficient CO2-fixing pyruvate:ferredoxin oxidoreductase (POR) complex and a high-affinity cbb3-type terminal oxidase increased under O2 limitation, suggesting a role in sustaining nitrite oxidation-driven autotrophy. This putatively more O2-sensitive POR complex might be protected from oxidative damage by Cu/Zn-binding superoxide dismutase, which also increased in abundance under low O2 conditions. Furthermore, the upregulation of proteins involved in alternative energy metabolisms, including Group 3b [NiFe] hydrogenase and formate dehydrogenase, indicate a high metabolic versatility to survive conditions unfavorable for aerobic nitrite oxidation. In summary, the genome and proteome of the first marine Nitrospira isolate identifies adaptations to life in the oxic ocean and provides insights into the metabolic diversity and niche differentiation of NOB in marine environments.

Description: We thank John B. Waterbury and Frederica Valois for providing the culture of Nitrospira marina Nb-295T and for continued advice about cultivation. The N. marina genome was sequenced as part of US Department of Energy Joint Genome Institute Community Sequencing Project 1337 to CLD, AES, and MAS in collaboration with the user community. We thank Claus Pelikan for bioinformatic assistance. This research was supported by a Simons Foundation Early Career Investigator in Marine Microbiology and Evolution Award (345889) and US National Science Foundation (NSF) award OCE-1924512 to AES. Proteomics analysis was supported by NSF awards OCE-1924554 and OCE-1850719, and NIH award R01GM135709 to MAS. BB was supported by the Austrian Science Fund (FWF) Project Number: J4426-B (“The influence of nitrifiers on the oceanic carbon cycle”), SL by the Netherlands Organization for Scientific Research (NWO) grant 016.Vidi.189.050, and CLD by NSF award OCE-125999.

Repository Name: Woods Hole Open Access Server

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