Specific Effect of Trace Metals on Marine Heterotrophic Microbial Activity and Diversity: Key Role of Iron and Zinc and Hydrocarbon-Degrading Bacteria

Marine microbes are an important control on the biogeochemical cycling of trace metals, but simultaneously, these metals can control the growth of microorganisms and the cycling of major nutrients like C and N. However, studies on the response/limitation of microorganisms to trace metals have traditionally focused on the response of autotrophic phytoplankton to Fe fertilization. Few reports are available on the response of heterotrophic prokaryotes to Fe, and even less to other biogeochemically relevant metals. We performed the first study coupling dark incubations with next generation sequencing to specifically target the functional and phylogenetic response of heterotrophic prokaryotes to Fe enrichment. Furthermore, we also studied their response to Co, Mn, Ni, Zn, Cu (individually and mixed), using surface and deep samples from either coastal or open-ocean waters. Heterotrophic prokaryotic activity was stimulated by Fe in surface open–ocean, as well as in coastal, and deep open-ocean waters (where Zn also stimulated). The most susceptible populations to trace metals additions were uncultured bacteria (e.g., SAR324, SAR406, NS9, and DEV007). Interestingly, hydrocarbon-degrading bacteria (e.g., Thalassolituus, Marinobacter, and Oleibacter) benefited the most from metal addition across all waters (regions/depths) revealing a predominant role in the cycling of metals and organic matter in the ocean.

[1]  R. Selvarajan,et al.  Distribution, Interaction and Functional Profiles of Epiphytic Bacterial Communities from the Rocky Intertidal Seaweeds, South Africa , 2019, Scientific Reports.

[2]  M. Göker,et al.  The Composite 259-kb Plasmid of Martelella mediterranea DSM 17316T–A Natural Replicon with Functional RepABC Modules from Rhodobacteraceae and Rhizobiaceae , 2017, Front. Microbiol..

[3]  Shicheng Chen,et al.  Dietary High Zinc Oxide Modulates the Microbiome of Ileum and Colon in Weaned Piglets , 2017, Front. Microbiol..

[4]  S. Khatiwala,et al.  Silicon and zinc biogeochemical cycles coupled through the Southern Ocean , 2017 .

[5]  S. Sørensen,et al.  Coping with copper: legacy effect of copper on potential activity of soil bacteria following a century of exposure. , 2016, FEMS microbiology ecology.

[6]  M. Doebeli,et al.  Decoupling function and taxonomy in the global ocean microbiome , 2016, Science.

[7]  P. Keeling,et al.  Diverse, uncultivated bacteria and archaea underlying the cycling of dissolved protein in the ocean , 2016, The ISME Journal.

[8]  D. Parry,et al.  Molecular screening of microbial communities for candidate indicators of multiple metal impacts in marine sediments from northern Australia , 2016, Environmental toxicology and chemistry.

[9]  Jay T. Lennon,et al.  Microbiomes in light of traits: A phylogenetic perspective , 2015, Science.

[10]  Sanjay K. Singh,et al.  Response of bacterioplankton to iron fertilization of the Southern Ocean, Antarctica , 2015, Front. Microbiol..

[11]  J. Gasol,et al.  Marine bacterial community structure resilience to changes in protist predation under phytoplankton bloom conditions , 2015, The ISME Journal.

[12]  R. Meena,et al.  Response of polar front phytoplankton and bacterial community to micronutrient amendments , 2015 .

[13]  F. Coulon,et al.  DECAPAGE PROJECT : HYDROCARBON DEGRADATION IN COASTAL SEDIMENTS * Dynamics and distribution of bacterial and archaeal communities in oil-contaminated temperate coastal mudflat mesocosms , 2015 .

[14]  Francisco P Chavez,et al.  Microbial community transcriptional networks are conserved in three domains at ocean basin scales , 2015, Proceedings of the National Academy of Sciences.

[15]  I. Obernosterer,et al.  Fe and C co-limitation of heterotrophic bacteria in the naturally fertilized region off the Kerguelen Islands , 2014 .

[16]  M. Ferrer,et al.  Alcanivorax borkumensis produces an extracellular siderophore in iron-limitation condition maintaining the hydrocarbon-degradation efficiency. , 2014, Marine genomics.

[17]  H. Vogel,et al.  Simultaneous Loss of Soil Biodiversity and Functions along a Copper Contamination Gradient: When Soil Goes to Sleep , 2014 .

[18]  A. Butler,et al.  Amphiphilic siderophore production by oil-associating microbes. , 2014, Metallomics : integrated biometal science.

[19]  I. Obernosterer,et al.  Effects of iron limitation on growth and carbon metabolism in oceanic and coastal heterotrophic bacteria , 2014 .

[20]  J. Lehtoranta,et al.  Iron–Manganese Concretions Sustaining Microbial Life in the Baltic Sea: The Structure of the Bacterial Community and Enrichments in Metal-Oxidizing Conditions , 2014 .

[21]  K. Bruland,et al.  Controls of Trace Metals in Seawater , 2013 .

[22]  Susan Holmes,et al.  phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data , 2013, PloS one.

[23]  T. Yokokawa,et al.  Bacterial Versus Archaeal Origin of Extracellular Enzymatic Activity in the Northeast Atlantic Deep Waters , 2013, Microbial Ecology.

[24]  Pelin Yilmaz,et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools , 2012, Nucleic Acids Res..

[25]  R. Amann,et al.  Microbial Community Response during the Iron Fertilization Experiment LOHAFEX , 2012, Applied and Environmental Microbiology.

[26]  Jennifer M. DeBruyn,et al.  Microbial control of diatom bloom dynamics in the open ocean , 2012 .

[27]  T. Berman,et al.  Prokaryotic community structure and respiration during long-term incubations , 2012, MicrobiologyOpen.

[28]  A. Rogers,et al.  Patterns of marine bacterioplankton biodiversity in the surface waters of the Scotia Arc, Southern Ocean. , 2012, FEMS microbiology ecology.

[29]  William A. Walters,et al.  Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms , 2012, The ISME Journal.

[30]  J. Groves,et al.  Alkane-oxidizing metalloenzymes in the carbon cycle. , 2011, Metallomics : integrated biometal science.

[31]  K. Timmis,et al.  Transcriptional profiling of the marine oil-degrading bacterium Alcanivorax borkumensis during growth on n-alkanes. , 2011, FEMS microbiology letters.

[32]  P. Hill,et al.  Did dilution limit the phytoplankton response to iron addition in HNLCLSi sub-Antarctic waters during the SAGE experiment? , 2011 .

[33]  Irina Dana Ofiteru,et al.  Combined niche and neutral effects in a microbial wastewater treatment community , 2010, Proceedings of the National Academy of Sciences.

[34]  J. Gasol,et al.  Prokaryotic carbon utilization in the dark ocean: growth efficiency, leucine-to-carbon conversion factors, and their relation , 2010 .

[35]  A. Tsuda,et al.  Temporal changes in community composition of heterotrophic bacteria during in situ iron enrichment in the western subarctic Pacific (SEEDS-II) , 2009 .

[36]  C. G. Wheat,et al.  Bacterial Variability within an Iron-Silica-Manganese-rich Hydrothermal Mound Located Off-axis at the Cleft Segment, Juan de Fuca Ridge , 2009 .

[37]  Mark D. Robinson,et al.  edgeR: a Bioconductor package for differential expression analysis of digital gene expression data , 2009, Bioinform..

[38]  E. Sintes,et al.  Prokaryotic extracellular enzymatic activity in relation to biomass production and respiration in the meso- and bathypelagic waters of the (sub)tropical Atlantic. , 2009, Environmental microbiology.

[39]  V. Orphan,et al.  Manganese- and Iron-Dependent Marine Methane Oxidation , 2009, Science.

[40]  Richard S. Lampitt,et al.  Southern Ocean deep-water carbon export enhanced by natural iron fertilization , 2009, Nature.

[41]  Yong-guan Zhu,et al.  Microbial DNA extraction and analyses of soil iron-manganese nodules , 2008 .

[42]  T. Healy,et al.  Transient wind‐driven coastal upwelling on a shelf with varying width and orientation , 2008 .

[43]  E. Delong,et al.  The Microbial Engines That Drive Earth's Biogeochemical Cycles , 2008, Science.

[44]  O. Zemb,et al.  Major differences of bacterial diversity and activity inside and outside of a natural iron-fertilized phytoplankton bloom in the Southern Ocean. , 2008, Environmental microbiology.

[45]  D. Lefèvre,et al.  Rapid bacterial mineralization of organic carbon produced during a phytoplankton bloom induced by natural iron fertilization in the Southern Ocean , 2008 .

[46]  A. Bricaud,et al.  Biochemical characteristics and bacterial community structure of the sea surface microlayer in the South Pacific Ocean , 2007 .

[47]  Peter N Golyshin,et al.  Obligate oil-degrading marine bacteria. , 2007, Current opinion in biotechnology.

[48]  B. Quéguiner,et al.  Effect of natural iron fertilization on carbon sequestration in the Southern Ocean , 2007, Nature.

[49]  E. Boyle,et al.  Mesoscale Iron Enrichment Experiments 1993-2005: Synthesis and Future Directions , 2007, Science.

[50]  N. Bhosle,et al.  Bacterial extracellular polymeric substance (EPS): a carrier of heavy metals in the marine food-chain. , 2006, Environment international.

[51]  H. Saito,et al.  Responses of phytoplankton and heterotrophic bacteria in the northwest subarctic Pacific to in situ iron fertilization as estimated by HPLC pigment analysis and flow cytometry , 2005 .

[52]  H. Ducklow,et al.  The heterotrophic bacterial response during the Southern Ocean Iron Experiment (SOFeX) , 2004 .

[53]  M. Weinbauer,et al.  Response of bacterioplankton to iron fertilization in the Southern Ocean , 2004 .

[54]  R. Walters,et al.  Circulation over the northeastern New Zealand continental slope, shelf and adjacent Hauraki Gulf, during spring and summer , 2004 .

[55]  J. Zeldis.  New and remineralised nutrient supply and ecosystem metabolism on the northeastern New Zealand continental shelf , 2004 .

[56]  S. Giovannoni,et al.  Cultivation and Growth Characteristics of a Diverse Group of Oligotrophic Marine Gammaproteobacteria , 2004, Applied and Environmental Microbiology.

[57]  F. Morel,et al.  Marine Bioinorganic Chemistry: The Role of Trace Metals in the Oceanic Cycles of Major Nutrients , 2003 .

[58]  F. Morel,et al.  The Biogeochemical Cycles of Trace Metals in the Oceans , 2003, Science.

[59]  P. Sutton,et al.  Absolute geostrophic currents in the East Auckland Current region , 2002 .

[60]  B. Quéguiner,et al.  Control of phytoplankton growth by iron and silicic acid availability in the subantarctic Southern Ocean: Experimental results from the SAZ Project , 2001 .

[61]  S. Cary.  Response of marine bacterial community composition to iron additions in three iron‐limited regimes , 2001 .

[62]  D. Janssen,et al.  Effects of Iron Limitation on the Degradation of Toluene by Pseudomonas Strains Carrying the TOL (pWWO) Plasmid , 2001, Applied and Environmental Microbiology.

[63]  E. Abraham,et al.  Internal tide dissipation, mixing, and vertical nitrate flux at the shelf edge of NE New Zealand , 2001 .

[64]  W. Cochlan.  The heterotrophic bacterial response during a mesoscale iron enrichment experiment (IronEx II) in the eastern equatorial Pacific Ocean , 2001 .

[65]  M. Cottrell,et al.  Carbon versus iron limitation of bacterial growth in the California upwelling regime , 2000 .

[66]  Josep M. Gasol,et al.  Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities , 2000 .

[67]  A. Butler,et al.  Self-assembling amphiphilic siderophores from marine bacteria. , 2000, Science.

[68]  H. Ducklow,et al.  Limitation of Bacterial Growth by Dissolved Organic Matter and Iron in the Southern Ocean , 2000, Applied and Environmental Microbiology.

[69]  N. M. Price,et al.  Utilization of iron bound to strong organic ligands by plankton communities in the subarctic Pacific Ocean , 1999 .

[70]  D. Hutchins,et al.  Size-fractionated biological iron and carbon uptake along a coastal to offshore transect in the NE Pacific , 1999 .

[71]  S. Ullrich,et al.  Profiles of ectoenzymes in the Indian Ocean: phenomena of phosphatase activity in the mesopelagic zone , 1999 .

[72]  B. Witholt,et al.  The PalkBFGHJKL Promoter Is under Carbon Catabolite Repression Control in Pseudomonas oleovorans but Not in Escherichia coli alk+Recombinants , 1999, Journal of bacteriology.

[73]  D. Roemmich,et al.  The mean and variability of ocean circulation past northern New Zealand: Determining the representativeness of hydrographic climatologies , 1998 .

[74]  J. Sharples,et al.  Tidal currents, mean flows, and upwelling on the north‐east shelf of New Zealand , 1998 .

[75]  Kenneth S. Johnson,et al.  Marine Chemistry Discussion Paper What controls dissolved iron concentrations in the world ocean , 1997 .

[76]  J. Sharples.  Cross-shelf intrusion of subtropical water into the coastal zone of northeast New Zealand , 1997 .

[77]  P. Tortell,et al.  The role of heterotrophic bacteria in iron-limited ocean ecosystems , 1996, Nature.

[78]  C. Lord.  Determination of trace metals in crude oil by inductively coupled plasma mass spectrometry with microemulsion sample introduction , 1991 .

[79]  R. Proctor,et al.  A numerical model investigation of the residual circulation in Hauraki Gulf, New Zealand , 1989 .

[80]  M. Starr,et al.  Metallic-Oxide encrustations of the nonprosthecate stalks of naturally occurring populations ofPlanctomyces bekefii , 1982, Current Microbiology.

[81]  H. Jannasch,et al.  Morphological Survey of Microbial Mats Near Deep-Sea Thermal Vents , 1981, Applied and environmental microbiology.

[82]  W. Maret.  Optical methods for measuring zinc binding and release, zinc coordination environments in zinc finger proteins, and redox sensitivity and activity of zinc-bound thiols. , 2002, Methods in enzymology.

[83]  D. Hutchins.  Response of marine bacterial community composition to iron additions in three iron-limited regimes , 2001 .

[84]  E. Stackebrandt,et al.  Microbial community dynamics in Mediterranean nutrient-enriched seawater mesocosms: changes in the genetic diversity of bacterial populations. , 2001, FEMS microbiology ecology.

[85]  J. Hall,et al.  The impact of in situ Fe fertilisation on the microbial food web in the Southern Ocean , 2001 .

[86]  I. Koike,et al.  High potential activity of extracellular alkaline phosphatase in deep waters of the central Pacific , 1997 .

[87]  F. Morel,et al.  Zinc and carbon co-limitation of marine phytoplankton , 1994, Nature.

[88]  David C. Smith,et al.  A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine , 1992 .

[89]  R. Weiner,et al.  Notes: Genus Hyphomonas Pongratz 1957 nom. rev. emend., Hyphomonas polymorpha Pongratz 1957 nom. rev. emend., and Hyphomonas neptunium (Leifson 1964) comb. nov. emend. (Hyphomicrobium neptunium) , 1984 .