Geobiology of marine magnetotactic bacteria

Abstract

Submitted in partial fulfillment of the requirements of the degree of Doctor of Philosophy in Biological Oceanography at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution June 2006Magnetotactic bacteria (MTB) biomineralize intracellular membrane-bound crystals of magnetite (Fe3O4) or greigite (Fe3S4), and are abundant in the suboxic to anoxic zones of stratified marine environments worldwide. Their population densities (up to 105 cells ml−1) and high intracellular iron content suggest a potentially significant role in iron cycling, but very little is known about their population dynamics and regulation by environmental geochemistry. The MTB community in Salt Pond (Falmouth, MA), a small stratified marine basin, was used as a model system for quantitative community studies. Magnetiteproducing MTB predominate slightly above the oxic-anoxic interface and greigiteproducing MTB predominate in sulfidic waters. A quantitative PCR (QPCR) assay was developed and applied to enumerate four major groups of MTB in Salt Pond: magnetite-producing cocci, barbells, the greigite-producing many-celled magnetotactic prokaryote (MMP), and a greigite-producing rod. The barbells were identified as δ-Proteobacteria while the rod was identified as the first MTB in the γ-Proteobacteria. The MMP, previously thought to be a single species, consists of at least five clades with greater than 5% divergence in their 16s rRNA. Fluorescent in situ hybridization probes showed significant variation in clade abundances across a seasonal cycle in salt marsh productivity. FISH also showed that aggregates consist of genetically identical cells. QPCR data indicated that populations are finely layered around the oxic-anoxic interface: cocci immediately above the dissolved Fe(II) peak, barbells immediately below, the MMP in microsulfidic waters, and the greigite-producing rod in low numbers (100 cells ml−1) below the gradient region. The barbell reached 1-10% of total eubacteria in the late season, and abundances of cocci and barbells appeared to vary inversely. Calculations based on qPCR data suggest that MTB are significant unrecognized contributors to iron flux in stratified environments. Barbells can respond to high oxygen levels by swimming toward geomagnetic south, the opposite of all previously reported magnetotactic behavior. This behavior is at least partially dependent on environmental oxidation-reduction potential. The co-existence of MTB with opposing polarities in the same redox environment conflicts with current models of the adaptive value of magnetotaxis.Funding for the research described in this thesis was provided by the Rinehart Coastal Research Center at WHOI, the WHOI Ocean Life Institute, and the WHOI Ocean Venture Fund