Article pubs.acs.org/est
Microbial Engineering of Floc Fe and Trace Element Geochemistry in a Circumneutral, Remote Lake Amy V. C. Elliott† and Lesley A. Warren*,† †
School of Geography and Earth Sciences, McMaster University, 1280 Main Street West, Hamilton, Ontario L8S 4K1, Canada S Supporting Information *
ABSTRACT: Evaluation of lacustrine floc Fe, Pb, and Cd biogeochemistry over seasonal (summer, winter) and water column depth (metalimnetic, hypolimnetic) scales reveals depth-independent seasonally significant differences in floc Fe biominerals and trace element (TE: Pb, Cd) sequestration, driven by floc microbial community shifts. Winter floc [TE] were significantly lower than summer [TE], driven by declining abundance and reactivity of floc amorphous Fe(III)-(oxy)hydroxide (FeOOH) phases under ice ([FeOOH]summer = 37−77 mgg−1 vs [FeOOH]winter = 0.3−7 mgg−1). Further, while high summer floc [FeOOH] was observed at both water column depths, winter floc was dominated by Fe(II) phases. However, the observed seasonal change in the nature and concentrations of floc Fe-phases was independent of water column [Fe], O2, and pH and, instead, significantly correlated to floc bacterial community membership. Bioinformatic modeling (Unifrac, PCA analyses) of in situ and experimental microcosm results identified a temperature-driven seasonal turnover of floc microbial communities, shifting from dominantly putative Fe metabolisms within summer floc to wintertime ancillary Fe reducing and S metabolizing bacteria. This seasonal shift of floc microbial community functioning, significantly the wintertime loss of microbial Fe(II)-oxidizing capability and concomitant increases of sulfur-reducing bacteria, alters dominant floc Fe minerals from Fe(III) to Fe(II) phases. This resulted in decreased winter floc [TE], not predicted by water column geochemistry.
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architecture and development,6,10,12 suggests that the resident floc microbial community will influence floc geochemistry in ways not currently captured by geochemical models, i.e., linkages among microbial metabolism and geochemical microenvironment development. Recent work has shown lacustrine floc aggregates as a distinct sedimentary system compartment, having a distinct geochemistry, microbiology, and composition from the bed sedimentary materials of wide ranging aquatic systems.4,5,13,14 Importantly, resident floc microbial communities were found to facilitate the concentration of TEs specifically through the collection/nucleation of highly reactive amorphous Fe(III)oxyhydroxide minerals (FeOOH), identifying a water column solid phase with differing controls over TE behavior than bed
INTRODUCTION The biogeochemistry of suspended sedimentary materials/ suspended particulate matter (SPM) has received a great deal of attention in the last several decades. This is due to the (i) ability of SPM to sequester large quantities of trace elements (TE) relative to bottom sediments, (ii) important role of SPM as a vector for TE transport, (iii) link SPM plays between the highly bioavailable aqueous phase and bed sediment (classical TE-sink) aquatic system compartments, and (iv) biologically flocculated nature of suspended particulates (i.e., “flocs”), such that flocs are regarded as mobile biofilms.1−8 Flocs may be derived from overland wash-off of soil aggregates, resuspended bottom sedimentary materials, and/or formed directly in suspension via a complex flocculation process.6 Regardless of their origin, the development and stabilization of suspended flocs are highly influenced by the activity of floc-colonizing bacteria and associated extracellular polymeric substances (EPS) (e.g., refs 6, and 9−11). The substantive biological nature of floc, as well as microbial influences on floc © 2014 American Chemical Society
Received: Revised: Accepted: Published: 6578
August 22, 2013 February 18, 2014 May 8, 2014 May 8, 2014 dx.doi.org/10.1021/es403754t | Environ. Sci. Technol. 2014, 48, 6578−6587
Environmental Science & Technology
Article
Figure 1. Seasonal geochemistry of (A) summer stratification and (B) winter stratification of Coldspring Lake, Algonquin Park, ON. Gray bars correspond to depth of suspended floc collection for each sampling campaign: 4.5 m (summer metalimnion) and 7.5 m (hypolimnion). Note differences in x-axes. TEM and EDS analyses revealed consistent association of floc microbial cells, and FeCd precipitates entrapped within organic EPS matrix within summer flocs (insert).
sedimentary materials.4,5 More recently, Elliott et al. (2014) demonstrated that collaborating putative Fe(III)-reducing (IRB) and Fe(II)-oxidizing (IOB) floc bacteria within consortial microaggregates (80 μm) couple Fe(III)-reduction with Fe(II)oxidation across diverse oxygenated (O2sat. = 1−103%) aquatic systems, not expected to sustain microbial Fe-metabolism. Steep microscale gradients in oxygen and pH under bulk oxic conditions have been similarly reported within marine snow and cyanobacterial colonies (macroscopic aggregates, >1 mm).15−19 Elliott et al. 2014 also demonstrated the formation and occurrence of reduced and oxidized Fe biominerals in floc; not expected under the bulk system oxic concentrations but reflective of interior aggregate low oxygen/anoxic conditions. This discovery suggests highly dynamic floc Fe-biogeochemistry, and therefore TE sequestration/mobilization, driven by microbial Fe-metabolism within the floc microhabitat. SPM and associated microbial communities will be exposed to highly differing physicochemical conditions as a function of water column depth as well as season. However, seasonal or depth-dependent changes in floc Fe/TE biogeochemistry or potential linkages to underlying floc microbial community functioning have yet to be investigated. Thus, the objectives of this investigation were to characterize floc: (i) bacterial community structure, (ii) Fe-geochemistry, (iii) Pb and Cd partitioning over depth and seasonal scales in a temperate, remote lake, and (iv) experimentally assess floc microbial FeIII/II-redox transformations under identified factors influencing floc biogeochemistry in situ. This was accomplished with an integrated biogeochemical approach, combining 454 16S amplicon sequencing, bioinformatics, and hierarchal clustering of whole bacterial communities, with Fe-bacterial enrichment
methodologies as well as solid phase TE and mineralogical analyses of floc aggregates to reveal biogeochemical linkages.
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MATERIALS AND METHODS
Field Investigation. Summer (2010-August) and winter (2011-March) sampling campaigns were conducted at Coldspring Lake; a remote, groundwater fed lake only accessible by float plane within the nature preserve area of Algonquin Park, ON, Canada (45°85′28″N 78°82′17″W) (Figure 1). This system was selected due to steep water column gradients in important variables known to regulate Fe-geochemistry during both summer and winter stratification periods ([O2], [Fe(II)], [Fe(total)], [S2−], [NO32−]) (Figure 1, Supporting Information (SI) Table S1). Further, very high hypolimnetic Feaq(II) and metalimnetic Feaq(III) (“dissolved”,
