How can microbial levels be controlled in the environment

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Delgado-Baquerizo, M. Microbial diversity drives multifunctionality in terrestrial ecosystems. Walker, T. Microbial temperature sensitivity and biomass change explain soil carbon loss with warming. We expand their analyses by varying pH from 1 to 14 and by including additional microbial redox reactions involved in the degradation of natural organic matter. These reactions include the oxidation of short-chain fatty acids and primary alcohols by proton reduction, iron reduction, and sulfate reduction.

Our analyses confirm the previous conclusion that changes in environmental pH directly alter energy available from redox reactions that produce or consume protons, and the significances of the changes depend on the numbers of protons produced or consumed Bethke et al.

Our simulation results also resonate with the previous studies that emphasize the indirect thermodynamic role of pH—pH affects chemical energies in the environment indirectly by affecting chemical speciation and thereby the concentrations of chemical species involved in microbial redox reactions Windman et al.

We often write stoichiometric reaction equations and compute their Gibbs free energy changes using the main chemical species at pH 7 Table 1 and Equation 1. By doing so, we implicitly account for the speciation effect at pH 7. But chemical speciation depends on pH, which impacts chemical reactions and their energies in two ways. First, chemical species participating in protonation and deprotonation have different concentrations at different pHs.

As a result, the main chemical species of pH 7 may give way to alternative forms at other pHs. Second, the stoichiometries of proton consumption and production are not fixed, but vary with pH. At a given pH, proton consumption and production depend on the relative significances of acids and their conjugate bases.

In response to pH variations, the concentrations of acids and their conjugate bases change Figure 1 and thus so do the stoichiometries of proton reactions. Consequently, for reactions that include proton consumption and production, the direct pH effect is not set but varies in magnitude with pH.

The indirect thermodynamic impact of pH is most notable for sulfate reduction by the oxidation of lactate, butyrate, and ethanol, and for acetoclastic methanogenesis reaction 16, 18, 20, and 22 in Table 1.

At pH 7, no proton would be produced or consumed by these reactions, and the available energies are not affected directly by pH. But according to the simulation results, their available energies vary significantly with the pH of the environment Figures 4D , 5B.

We account for the variations using pH-dependent chemical speciation—these reactions involve bicarbonate, sulfide, and other chemical species, whose concentrations vary significantly with pH. Figures 2 — 5 compare the direct and the total thermodynamic impacts of pH the dashed and solid lines, respectively. The differences between the two lines highlight the indirect energy contribution by chemical speciation.

Two patterns arise from these figures. First, microbial thermodynamic responses are not uniform. The available energies of syntrophic oxidation reactions increase with increasing pH. For hydrogenotrophic sulfate reduction and methanogenesis, their available energies decrease with increasing pH. For other microbial redox reactions, in response to pH increases, available energies first decrease and then, after reaching minimum values, begin to increase.

These heterogeneous responses arise in part from the indirect speciation impact of pH. The speciation impact is not consistent throughout the entire pH range of 1— For example, for redox reactions that produce bicarbonate, energy available always increases as pH moves away from 7, regardless of whether pH is increasing or decreasing.

As a second example, the speciation of ferrous iron only affects significantly the available energy of iron reduction at pH above 9. At lower pHs, the speciation impact is negligible. Second, microbial iron reduction stands out from the other reactions in its strong response to pH. Energy available from the reduction of iron oxides and hydroxides depends significantly on pH.

This sensitivity reflects consumption of relatively large numbers of protons, from Microbial thermodynamic responses to pH lead to a cascade of metabolic effects, including impacts to the thermodynamic drives of respiration. We took butyrate syntrophic oxidation, and acetotrophic and hydrogenotrophic iron reduction, sulfate reduction, and methanogenesis as examples, and analyzed how environmental pH controls the thermodynamic drives and hence the rates of these reactions in the assumed freshwater environment.

Like the energies available in the environment, the thermodynamic drives of different microbial respiration reactions respond differently to changes in pH.

Specifically, a pH increase from 1 to 14 raises the thermodynamic drive of syntrophic butyrate oxidation from negative to positive and hence moves the reaction from thermodynamically unfavorable to favorable. On the other hand, increasing pH changes iron reduction and hydrogenotrophic methanogenesis from thermodynamically favorable to unfavorable. It should be made clear that our thermodynamic drive calculations are specific for the assumed environment.

In an environment of different geochemical conditions, thermodynamic drives may be different, and hence pH variations may modify respiration rates to different extents. For example, in the hypothetical solution, pH variation does not change much the thermodynamic potential factor of acetoclastic methanogenesis, and hence has little influence on the rate of the process Figure 7D. At pH between 5. But the pattern in the responses of the thermodynamic drive should be similar, regardless of the concentration of methane or other chemical compounds.

As shown in Figure 6D , the thermodynamic drive always increases as pH moves away from 7. The pH limits of microbial metabolisms are a classical physiological parameter. Previous studies have attributed these pH limits to different physiological mechanisms, including cellular structures and metabolisms. First, both acidophiles and alkaliphiles need to employ unique surface structures to develop acid or alkaline tolerance.

For example, the cell walls of alkaliphiles have acidic polymers, which may protect cells from hydroxide ions Horikoshi, Acidophiles, such as the members of Ferroplasma , mix caldarchaetidylglycerol tetraether lipids into their membranes to make a barrier to protons in the environment Golyshina and Timmis, Acidic or alkaline conditions also present a challenge to cell metabolism. For both acidophiles and alkaliphiles, cytoplasmic pH is often closer to neutral pH than the environments Lowe et al.

Maintaining a pH gradient across the membrane consumes energy Booth, In addition, under acidic conditions, conjugate acids become significant in the environment, and diffuse through the cell membrane, which destabilizes the membrane and dissipates proton motive force Russell, Very low or high pH levels also interfere with solute transport across the membrane and energy conservation by respiration Matin, ; Krulwich et al. Our thermodynamic analyses show that environmental pH affects the thermodynamics of microbial redox reactions, and determines whether microbial respiration reactions are thermodynamically favorable or not.

Therefore, in addition to microbial physiology, the pH limits may arise, at least in part, from the response of reaction thermodynamics to pH. For example, reaction thermodynamics sets the lower pH limit for syntrophic butyrate oxidizers. In the assumed environment, syntrophic butyrate oxidation becomes thermodynamically unfavorable and thus stops at pH below 5. In laboratory experiments, both butyrate and acetate have relatively large concentrations Dwyer et al.

The predicted pH limits are consistent with previous laboratory observations. For example, S. Its close relatives, including S. As a second example, the thermodynamics of iron reduction sets the upper limit for microbes reducing ferric oxides and oxyhydroxides. In the assumed environment, at pH above 7. In laboratory reactors, H 2 , acetate, and ferrous iron often have concentrations orders magnitude above the concentrations in the assumed environment.

The upper pH limit for iron reduction depends on ferric minerals Postma and Jakobsen, For example, if we choose natural ferrihydrite as an electron acceptor, acetotrophic reduction of ferrihydrite becomes thermodynamically unfavorable at pH 8. This upper limit is consistent with the value determined using laboratory experiments. Straub et al. By promoting or inhibiting microbial redox reactions, environmental pH is capable of shaping the interactions between microbial groups.

For example, previous studies of microbial syntrophy have emphasized the importance of H 2 levels of the environment—a key parameter that dictates the thermodynamics and occurrence of syntrophic degradation Schink, The above results show that like H 2 levels, pH can change the thermodynamic status and rates of syntrohic oxidation of short-chain fatty acids and primary alcohols, and hence determine the occurrence and significance of these processes in the environment.

By promoting or inhibiting microbial respiration, environmental pH is also capable of shaping microbial community composition. Microbial iron reduction and sulfate reduction, for example, occur widely in subsurface environments and compete against each other for the common electron donors of H 2 and acetate. The current paradigm describing their interactions follows the tragedy of commons and assumes that iron reducers hold either a thermodynamic or kinetic advantage and as a result, always win the competition against sulfate reducers Chapelle and Lovley, ; Bethke et al.

Our modeling results show that the competitive advantage of iron reducers is pH dependent. Specifically, the thermodynamic drive of microbial iron reduction responds significantly to pH. In the assumed environment, that response lowers iron reduction rates from maximum values to 0 over a narrow pH range of 1 unit.

In comparison, sulfate reduction responds relatively modestly to pH and stays thermodynamically favorable over the entire pH range between 1 and These results suggest iron reducers can win the competition against sulfate reducers under acidic conditions but might lose the competition under alkaline conditions. Thus, changes in pH have the potential to alter the proportions of iron reducers relative to sulfate reducers in an environment. Results of laboratory experiments by Kirk et al.

In their study, microbial consortia from a freshwater aquifer grew on acetate under two different pHs, 7. The relative abundance of sequences that grouped within Geobacteraceae and Myxococcaceae was twice as high in pH 5.

Members of Geobacteraceae and Myxococcaceae , such as Geobacter and Anaeromyxobacter , are capble of iron reduction Lonergan et al. Conversely, sequences that grouped within taxa commonly associated with sulfate reduction, such as Desulfobulbaceae, Desulfovibrionaceae, Desulfuromonadaceae , and Desulfobacteraceae , were primarly only present in pH 7.

These differences in relative abundance are consistent with contributions of iron reduction and sulfate reduction to acetate oxidation evaluated using mass-balance calculations. According to their results, in pH 7. At pH 5. In agreement with these findings, furthermore, Kirk et al. We applied geochemical reaction modeling, and explored the thermodynamic responses of microbial redox reactions to environmental pH.

Our modeling focused on the energy yields of redox reactions, and neglected other impacts brought upon cell metabolisms by pH. For example, low pH conditions promotes the diffusion of formic acid, acetic acid, and other short-chain fatty acids across the membrane, which dissipates proton motive force across the membrane and inhibits microbial growth Russell, Low pH also helps dissolve ferric and ferrous minerals, which makes available ferric iron to iron reducers and ferrous iron to iron oxidizers, and promotes the biogeochemical cycling of iron Coupland and Johnson, ; Emerson et al.

Our work represents a step forward toward a mechanistic view of the pH control on microbial metabolisms and community structures. Current studies rely on phenomenological models to describe the apparent microbial responses to pH.

Here we focused on microbial respiration, and illustrated that environmental pH influences the thermodynamics of microbial redox reactions and that this influence can be strong enough to cause significant changes in respiration kinetics.

The simulation results illustrate that environmental pH can impact the energies of microbial redox reactions in two ways. Chemical energies are a direct function of pH—the chemical activity of protons—for reactions that consume and produce protons.

In addition, pH also controls the speciation and concentrations of electron donors, acceptors, and reaction products, which in turn determine the energy yields of redox reactions. For microbial reduction of goethite and other ferric oxyhydroxides, the effect of proton consumption is dominant. For other reactions, the indirect speciation effect is of similar magnitude as the proton activity effect.

These thermodynamic responses are strong enough that they can switch the thermodynamic states of microbial respiration between favorable and unfavorable and change microbial rates from 0 to their maximum values. Thermodynamic responses also help give rise to the lower or upper pH limits of microbial respiration reactions and pH-dependent changes in microbial community composition.

By changing the thermodynamics of individual microbial redox reactions, pH variations are capable of shifting microbial community structures and modulating the interactions among microbes.

Taken together, our results provide a mechanistic understanding of how environmental pH regulates microbial respiration and affects the community composition of natural microbes.

They expand our view on the evaluation of microbial processes using routine environmental parameters, such as pH and chemical energies. In addition to microbial respiration, microbial growth, and maintenance are also influenced by environmental pH Russell and Dombrowski, Future efforts should explore the pH impact on growth and maintenance in order to achieve a holistic view of microbial response to environmental pH.

QJ and MK designed the research. QJ carried out the simulation, and wrote the first draft of the manuscript, and MK revised the manuscript. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Amend, A. Macroecological patterns of marine bacteria on a global scale.

Baker-Austin, C. Life in acid: pH homeostasis in acidophiles. Trends Microbiol. Bennett, P. Silicates, silicate weathering, and microbial ecology. Bethke, C. Geochemical and Biogeochemical Reaction Modeling, 2nd Edn. Box Preliminary concerns for conducting air sampling Consider the possible characteristics and conditions of the aerosol, including size range of particles, relative amount of inert material, concentration of microorganisms, and environmental factors.

Determine the type of sampling instruments, sampling time, and duration of the sampling program. Determine the number of samples to be taken. Ensure that adequate equipment and supplies are available. Determine the method of assay that will ensure optimal recovery of microorganisms.

Select a laboratory that will provide proper microbiologic support. Ensure that samples can be refrigerated if they cannot be assayed in the laboratory promptly. Sampling methods and descriptions and samplers for each. Example use: sampling water aerosols to Legionella spp. Buffered gelatin, tryptose saline, peptone, nutrient broth Ambient temperature and humidity will influence length of collection time Chemical Corps.

All Glass Impinger AGI Impaction on solid surfaces Air drawn into the sampler; particles deposited on a dry surface Viable particles; viable organisms on non-nutrient surfaces, limited to organisms that resist drying and spores ; size measurement, and concentration over time.

Example use: sampling air for Aspergillus spp. Sieve impactors can be set up to measure particle size. Slit impactors have a rotating support stage for agar plates to allow for measurement of concentration over time. Example uses: sampling air for bacteria in the vicinity of and during a medical procedure; general measurements of microbial air quality. Settle plates Filtration Air drawn through a filter unit; particles trapped; 0.

Example use: air sampling for Aspergillus spp. Biotest RCS Plus Electrostatic precipitation Air drawn over an electro- statically charged surface; particles become charged Viable particles; viable organisms on non-nutrient surfaces, limited to spores and organisms that resist drying ; concentration over time Solid collecting surfaces glass, and agar 85 Yes High volume sampling rate, but equipment is complex and must be handled carefully; not practical for use in health- care settings.

Chemical solutions and recommended concentration in water. Environmental surface sampling methods, descriptions, standards and references. Get Email Updates. To receive email updates about this page, enter your email address: Email Address. What's this? Return to Guidelines Library. Links with this icon indicate that you are leaving the CDC website. Linking to a non-federal website does not constitute an endorsement by CDC or any of its employees of the sponsors or the information and products presented on the website.

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Cancel Continue. Viable organisms, and concentration over time. Antifoaming agent may be needed. Ambient temperature and humidity will influence length of collection time. Viable particles; viable organisms on non-nutrient surfaces, limited to organisms that resist drying and spores ; size measurement, and concentration over time.

Available as sieve impactors or slit impactors. Viable particles. Simple and inexpensive; best suited for qualitative sampling; significant airborne fungal spores are too buoyant to settle efficiently for collection using this method.

Viable particles; viable organisms on non-nutrient surfaces, limited to spores and organisms that resist drying ; concentration over time.

Calibration is difficult and is done only by the factory; relative comparison of airborne contamination is its general use.

On surfaces in the environment? Microbial levels on skin are best controlled by hand washing, on surfaces in the environment with use of disinfectants like bleach, and in the air by HEPA filtration systems. Exercise 7 Ubiquity of Bacteria 1. Why do you suppose this habitat contains such a high microbial count? Were any plates completely lacking in colonies?

Do you think that the habitat sampled was really sterile?