Ecological succession among iron-oxidizing bacteria

Abstract

Despite over 125 years of study, the factors that dictate species dominance in neutrophilic iron-oxidizing bacterial (FeOB) communities remain unknown. In a freshwater wetland, we documented a clear ecological succession coupled with niche separation between the helical stalk-forming Gallionellales (for example, Gallionella ferruginea) and tubular sheath-forming Leptothrix ochracea. Changes in the iron-seep community were documented using microscopy and cultivation-independent methods. Quantification of Fe-oxyhydroxide morphotypes by light microscopy was coupled with species-specific fluorescent in situ hybridization (FISH) probes using a protocol that minimized background fluorescence caused by the Fe-oxyhydroxides. Together with scanning electron microscopy, these techniques all indicated that Gallionellales dominated during early spring, with L. ochracea becoming more abundant for the remainder of the year. Analysis of tagged pyrosequencing reads of the small subunit ribosomal RNA gene (SSU rRNA) collected during seasonal progression supported a clear Gallionellales to L. ochracea transition, and community structure grouped according to observed dominant FeOB forms. Axis of redundancy analysis of physicochemical parameters collected from iron mats during the season, plotted with FeOB abundance, corroborated several field and microscopy-based observations and uncovered several unanticipated relationships. On the basis of these relationships, we conclude that the ecological niche of the stalk-forming Gallionellales is in waters with low organic carbon and steep redoxclines, and the sheath-forming L. ochracea is abundant in waters that contain high concentrations of complex organic carbon, high Fe and Mn content and gentle redoxclines. Finally, these findings identify a largely unexplored relationship between FeOB and organic carbon.

Microbial Iron Oxidation in the Arctic Tundra and Its Implications for Biogeochemical Cycling

“…Somewhat surprisingly, the overall relative abundance of Gallionellales and Leptothrix spp. ranged from 3 to 10%, whereas in temperate iron seeps, these groups may account for between 25 and 50% of the total population (18,21,22). It is not clear why the abundances of known FeOB are reduced in these tundra iron mats.…”

“…5). The specific reasons for clustering of the TFS samples with the early successional community in Maine are not understood; however, the average temperature was 11°C for the early season community in Maine, similar to the temperature for TFS sites, while later in the season, the temperature in Maine rose to 15 to 18°C (18). A more complete analysis of the microbiome (13 sites and 40 samples) of microbial iron mats from Maine, Virginia, Texas, and Wyoming and in Denmark found that TFS iron mats cluster much more closely to these other circumneutral terrestrial sites than they do to iron-oxidizing communities from acidic (pH Ͻ4) or marine environments (J. J. Scott and D. Emerson, unpublished data).…”

Assessing Biomineral Formation by Iron‐oxidizing Bacteria in a Circumneutral Creek

“…These processes commonly occur simultaneously upon mixing of iron-rich, anoxic groundwater with oxygen-rich surface water (Druschel et al 2008). Iron biomineral formation from microbially mediated processes has been identified in diverse aqueous environments, including acid mine drainage sites (Colmer et al 1950;Baker et al 2009;Johnson and Hallberg 2015), hydrothermal vents (Emerson et al 1999;Peng et al 2011;Toner et al 2012), and circumneutral pH surface waters (Emerson and Moyer 1997;Duckworth et al 2009;Emerson et al 2010;Fleming et al 2014). In many circumneutral pH waters, abiotic oxidation is in direct competition with neutrophilic iron oxidizing bacteria (FeOB), organisms that exist at oxic-anoxic interfaces and have metabolic capabilities that promote rapid iron oxidation (Druschel et al 2008).…”

“…In many circumneutral pH waters, abiotic oxidation is in direct competition with neutrophilic iron oxidizing bacteria (FeOB), organisms that exist at oxic-anoxic interfaces and have metabolic capabilities that promote rapid iron oxidation (Druschel et al 2008). Multiple neutrophilic, microaerophilic FeOB, such as Leptothrix, Gallionella, and Sideroxydans, have been identified and studied to understand biotic-abiotic interactions in diverse environments (Duckworth et al 2009;Fleming et al 2014).…”

“…The importance of FeOB and iron oxides originates from their sorptive capacity and influence on delivered water quality in distribution systems through pipe oxidation (Cullimore and McCann 1978;Søgaard et al 2001;Fleming et al 2014;Sowers et al 2017), importance in microbial…”