Iron oxidation stimulates organic matter decomposition in humid tropical forest soils

Glob Chang Biol. 2013 Sep;19(9):2804-13. doi: 10.1111/gcb.12229. Epub 2013 Jul 14.

Abstract

Humid tropical forests have the fastest rates of organic matter decomposition globally, which often coincide with fluctuating oxygen (O2 ) availability in surface soils. Microbial iron (Fe) reduction generates reduced iron [Fe(II)] under anaerobic conditions, which oxidizes to Fe(III) under subsequent aerobic conditions. We demonstrate that Fe (II) oxidation stimulates organic matter decomposition via two mechanisms: (i) organic matter oxidation, likely driven by reactive oxygen species; and (ii) increased dissolved organic carbon (DOC) availability, likely driven by acidification. Phenol oxidative activity increased linearly with Fe(II) concentrations (P < 0.0001, pseudo R(2) = 0.79) in soils sampled within and among five tropical forest sites. A similar pattern occurred in the absence of soil, suggesting an abiotic driver of this reaction. No phenol oxidative activity occurred in soils under anaerobic conditions, implying the importance of oxidants such as O2 or hydrogen peroxide (H2 O2 ) in addition to Fe(II). Reactions between Fe(II) and H2 O2 generate hydroxyl radical, a strong nonselective oxidant of organic compounds. We found increasing consumption of H2 O2 as soil Fe(II) concentrations increased, suggesting that reactive oxygen species produced by Fe(II) oxidation explained variation in phenol oxidative activity among samples. Amending soils with Fe(II) at field concentrations stimulated short-term C mineralization by up to 270%, likely via a second mechanism. Oxidation of Fe(II) drove a decrease in pH and a monotonic increase in DOC; a decline of two pH units doubled DOC, likely stimulating microbial respiration. We obtained similar results by manipulating soil acidity independently of Fe(II), implying that Fe(II) oxidation affected C substrate availability via pH fluctuations, in addition to producing reactive oxygen species. Iron oxidation coupled to organic matter decomposition contributes to rapid rates of C cycling across humid tropical forests in spite of periodic O2 limitation, and may help explain the rapid turnover of complex C molecules in these soils.

Keywords: carbon cycle; iron oxidation; iron reduction; oxidative enzyme; oxygen; soil organic matter; soil respiration; tropical forest.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Biodegradation, Environmental
  • Carbon Dioxide / metabolism
  • Humidity*
  • Iron / metabolism*
  • Oxidation-Reduction
  • Phenols / metabolism
  • Soil / chemistry*
  • Trees*
  • Tropical Climate*

Substances

  • Phenols
  • Soil
  • Carbon Dioxide
  • Iron