Redox Fluctuation Structures Microbial Communities in a Wet Tropical Soil

Abstract

Frequent high-amplitude redox fluctuation may be a strong selective force on the phylogenetic and physiological composition of soil bacterial communities and may promote metabolic plasticity or redox tolerance mechanisms. To determine effects of fluctuating oxygen regimens, we incubated tropical soils under four treatments: aerobic, anaerobic, 12-h oxic/anoxic fluctuation, and 4-day oxic/anoxic fluctuation. Changes in soil bacterial community structure and diversity were monitored with terminal restriction fragment length polymorphism (T-RFLP) fingerprints. These profiles were correlated with gross N cycling rates, and a Web-based phylogenetic assignment tool was used to infer putative community composition from multiple fragment patterns. T-RFLP ordinations indicated that bacterial communities from 4-day oxic/anoxic incubations were most similar to field communities, whereas those incubated under consistently aerobic or anaerobic regimens developed distinctly different molecular profiles. Terminal fragments found in field soils persisted either in 4-day fluctuation/aerobic conditions or in anaerobic/12-h treatments but rarely in both. Only 3 of 179 total fragments were ubiquitous in all soils. Soil bacterial communities inferred from in silico phylogenetic assignment appeared to be dominated by Actinobacteria (especially Micrococcus and Streptomycetes), "Bacilli," "Clostridia," and Burkholderia and lost significant diversity under consistently or frequently anoxic incubations. Community patterns correlated well with redox-sensitive processes such as nitrification, dissimilatory nitrate reduction to ammonium (DNRA), and denitrification but did not predict patterns of more general functions such as N mineralization and consumption. The results suggest that this soil's indigenous bacteria are highly adapted to fluctuating redox regimens and generally possess physiological tolerance mechanisms which allow them to withstand unfavorable redox periods.Oxygen is the primary terminal electron acceptor for the respiratory processes of most upland soil microorganisms (41); it is a critical determinant of both soil redox status and the physiological pathways available to bacteria and fungi mediating C and N cycles. As soil redox (pE) decreases, dominant element transformations are generally assumed to shift in a well-defined succession from high-energy-yield processes to those that release less energy for microbial growth. This idea, that biological metabolism should follow the electrochemical constraints of a system, is a relatively old concept; it was first described in 1960 (1) and later supported by studies of waterlogged sediments, aquifers (11, 32), and rice paddies (56). In all of these cases, changes in redox potential occur gradually over time and/or space.In upland humid tropical forests, soils have been found to experience rapid redox fluctuations (51). In these ecosystems, the combination of high C availability, warm temperatures, abundant rainfall, clay soils with high water-holding capacity, and high metaboli...

When Wet Gets Wetter: Decoupling of Moisture, Redox Biogeochemistry, and Greenhouse Gas Fluxes in a Humid Tropical Forest Soil

“…Our 24-day water-addition treatment represents an extreme but plausible end-member of potential rainfall scenarios. Dominant redox processes can shift over scales of days to weeks in wetland ecosystems (Achtnich and others 1995;Ratering and Conrad 1998), and we predicted similar rapid responses in our tropical forest ecosystem given the facultative anaerobic capacity of the endemic microbial community (Pett-Ridge and Firestone 2005). We compared patterns in the concentrations of electron acceptors (O 2 , NO 3 , and SO 4 ) and reduced products (Mn(II), Fe(II), and soil CH 4 ) as relative indicators of redox reactions.…”

“…The response of humid tropical forest soil microbial communities to variation in moisture and O 2 availability could be distinct from that of temperate ecosystems. In soil from our site, microbial biomass and taxonomic richness were greatest under conditions of fluctuating O 2 availability relative to static aerobic conditions (Pett-Ridge and Firestone 2005). From a microbial perspective, consistently high soil moisture could represent an appropriate reference condition in this ecosystem, whereas declines in moisture might impose greater stress.…”

Plant and Microbial Controls on Nitrogen Retention and Loss in a Humid Tropical Forest

“…Plots were located within a 1 km 2 area at 650-750 m elevation. The TMF 2 and 4 plots are part of on-going studies of N and C cycling in humid tropical forest soils (Silver et al 1999, 2005, Pett-Ridge and Firestone 2005, Teh et al 2005, Pett-Ridge et al 2006. The TMF Icacos site is part of a long-term study of catchment-scale N cycling (McDowell et al 1992).…”

Comparison of Two Fingerprinting Techniques, Terminal Restriction Fragment Length Polymorphism and Automated Ribosomal Intergenic Spacer Analysis, for Determination of Bacterial Diversity in Aquatic Environments

“…About 50 ng of purified 16S rRNA gene amplicons from each of the two duplicate PCRs were digested separately in a 20-l reaction volume that contained 10 U of the enzyme AluI (Promega) at 37°C for 3 h. This specific restriction enzyme was selected because previous studies demonstrated that it is highly efficient in assessing phylotype richness and bacterial diversity in aquatic assemblages (27,30,34). One single restriction enzyme was utilized here for T-RFLP analysis, as several investigations demonstrated that the use of two or more restriction enzymes can produce differences in the community composition (31) but not in term of phylotype richness and diversity estimates based on different indices (13,15,19,44).…”