Microorganisms have a variety of evolutionary adaptations and physiological acclimation mechanisms that allow them to survive and remain active in the face of environmental stress. Physiological responses to stress have costs at the organismal level that can result in altered ecosystem-level C, energy, and nutrient flows. These large-scale impacts result from direct effects on active microbes' physiology and by controlling the composition of the active microbial community. We first consider some general aspects of how microbes experience environmental stresses and how they respond to them. We then discuss the impacts of two important ecosystem-level stressors, drought and freezing, on microbial physiology and community composition. Even when microbial community response to stress is limited, the physiological costs imposed on soil microbes are large enough that they may cause large shifts in the allocation and fate of C and N. For example, for microbes to synthesize the osmolytes they need to survive a single drought episode they may consume up to 5% of total annual net primary production in grassland ecosystems, while acclimating to freezing conditions switches Arctic tundra soils from immobilizing N during the growing season to mineralizing it during the winter. We suggest that more effectively integrating microbial ecology into ecosystem ecology will require a more complete integration of microbial physiological ecology, population biology, and process ecology.

Microbial stress‐response physiology and its implications for ecosystem function

Dormancy is a bet-hedging strategy used by a wide range of taxa, including microorganisms. It refers to an organism's ability to enter a reversible state of low metabolic activity when faced with unfavourable environmental conditions. Dormant microorganisms generate a seed bank, which comprises individuals that are capable of being resuscitated following environmental change. In this Review, we highlight mechanisms that have evolved in microorganisms to allow them to successfully enter and exit a dormant state, and discuss the implications of microbial seed banks for evolutionary dynamics, population persistence, maintenance of biodiversity, and the stability of ecosystem processes.

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Microbial seed banks: the ecological and evolutionary implications of dormancy

Many bacteria, including a variety of important human pathogens, are known to respond to various environmental stresses by entry into a novel physiological state, where the cells remain viable, but are no longer culturable on standard laboratory media. On resuscitation from this ‘viable but nonculturable’ (VBNC) state, the cells regain culturability and the renewed ability to cause infection. It is likely that the VBNC state is a survival strategy, although several interesting alternative explanations have been suggested. This review describes the VBNC state, the various chemical and physical factors known to induce cells into this state, the cellular traits and gene expression exhibited by VBNC cells, their antibiotic resistance, retention of virulence and ability to attach and persist in the environment, and factors that have been found to allow resuscitation of VBNC cells. Along with simple reversal of the inducing stresses, a variety of interesting chemical and biological factors have been shown to allow resuscitation, including extracellular resuscitation-promoting proteins, a novel quorum-sensing system (AI-3) and interactions with amoeba. Finally, the central role of catalase in the VBNC response of some bacteria, including its genetic regulation, is described.

Recent findings on the viable but nonculturable state in pathogenic bacteria.

Ageing results from complex genetically and epigenetically programmed processes that are elicited in part by noxious or stressful events that cause programmed cell death Here, we report that administration of spermidine, a natural polyamine whose intracellular concentration declines during human ageing, markedly extended the lifespan of yeast, flies and worms, and human immune cells In addition, spermidine administration potently inhibited oxidative stress in ageing mice In ageing yeast, spermidine treatment triggered epigenetic deacetylation of histone H3 through inhibition of histone acetyltransferases (HAT), suppressing oxidative stress and necrosis Conversely, depletion of endogenous polyamines led to hyperacetylation, generation of reactive oxygen species, early necrotic death and decreased lifespan The altered acetylation status of the chromatin led to significant upregulation of various autophagy-related transcripts, triggering autophagy in yeast, flies, worms and human cells Finally, we found that enhanced autophagy is crucial for polyamine-induced suppression of necrosis and enhanced longevity

Induction of autophagy by spermidine promotes longevity

Examinination of microbial diversity in environments of increasing salt concentrations indicates that certain types of dissimilatory metabolism do not occur at the highest salinities. Examples are methanogenesis for H2 + CO2 or from acetate, dissimilatory sulfate reduction with oxidation of acetate, and autotrophic nitrification. Occurrence of the different metabolic types is correlated with the free-energy change associated with the dissimilatory reactions. Life at high salt concentrations is energetically expensive. Most bacteria and also the methanogenic archaea produce high intracellular concentrations of organic osmotic solutes at a high energetic cost. All halophilic microorganisms expend large amounts of energy to maintain steep gradients of NA+ and K+ concentrations across their cytoplasmic membrane. The energetic cost of salt adaptation probably dictates what types of metabolism can support life at the highest salt concentrations. Use of KCl as an intracellular solute, while requiring far-reaching adaptations of the intracellular machinery, is energetically more favorable than production of organic-compatible solutes. This may explain why the anaerobic halophilic fermentative bacteria (order Haloanaerobiales) use this strategy and also why halophilic homoacetogenic bacteria that produce acetate from H2 + CO2 exist whereas methanogens that use the same substrates in a reaction with a similar free-energy yield do not.

Bioenergetic Aspects of Halophilism

A new strictly anaerobic, alkaliphilic, moderately thermophilic, fermentative, spore-forming bacterium, strain K1T, was isolated from manure samples (pH 6-8). Cells were Gram-positive, straight, non-motile rods that grew at temperatures of 37-66 degrees C (optimum at 62 degrees C) and in a pH range of 8.0-10.5 (optimum at 9.5-9.7). The bacterium fermented D-glucose, sucrose, D-fructose, D-trehalose and starch as carbon and energy sources. It required vitamins and its growth is stimulated by yeast extract. The major metabolic products were H2 and acetate. Cells were catalase-negative and could reduce nitrate to nitrite. The G+C content of the DNA was 42.2 mol%. Based on the phenotypic properties and 16S rDNA sequencing and DNA-DNA hybridization data, strain K1T (= DSM 12423T = ATCC 700785T = VKM B-2193T) was assigned to the new genus Anoxybacillus gen. nov., as a representative of a new species, Anoxybacillus pushchinensis sp. nov. 'Bacillus flavothermus' strain d.y., which was found to be closely related to strain K1T, is described as Anoxybacillus flavithermus comb. nov. (type strain = d.y.T = DSM 2641T).

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Anoxybacillus pushchinensis gen. nov., sp. nov., a novel anaerobic, alkaliphilic, moderately thermophilic bacterium from manure, and description of Anoxybacillus flavitherms comb. nov.

Cultivation of Mycobacterium smegmatis cells in a nitrogen-limited minimal medium (SR-1) followed by prolonged storage at room temperature without shaking resulted in the gradual accumulation of morphologically distinct ovoid forms characterized by (i) low metabolic activity; (ii) elevated resistance to antibiotics and to heat treatment; and (iii) inability to produce colonies on standard agar plates (non-platable cells). Detailed microscopic examination confirmed that ovoid cells possessed an intact cell envelope, specific fine structure and large electron-transparent bodies in the cytoplasm. Cell staining with Nile red and analysis of the lipid content by TLC revealed the presence of significant amounts of apolar lipids in these bodies. The ovoid forms could be stored for significant periods (up to 5 months) and resuscitated afterwards in a modified Sauton's medium. Importantly, resuscitation of ovoid cells was accompanied by their transformation into the typical rod-shaped cells. We suggest that the observed ovoid cells represent dormant forms, resembling morphologically distinct cells of Mycobacterium tuberculosis previously isolated from tuberculosis patients and infected animals.

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Dormant forms of Mycobacterium smegmatis with distinct morphology

Information about the functions of extracellular autoregulators, which adapt microorganisms to the stresses “scheduled” in the development cycle of microbial cultures (stresses of new medium, starvation, or space exhaustion (high cell density)) is summarized in the review. In a number of bacteria and yeasts, derivatives of alkylhydroxybenzenes (AHB), particularly of the class of alkyl resorcinols, act as autoregulators with adaptogenic functions. The chemical structure of AHB determines their amphiphility; capacity for physical and chemical interaction with membrane lipids, proteins, and DNA; properties as natural modifiers of biological membranes and enzymes; and the expression of antioxidant activity. Increase of AHB concentration up to the critical level (10−5-10−4 M) results in cessation of cell division and in transition of the microbial culture to the stationary phase; further increase to 10−4-10−3 M induces a transition of some of the cells of a post-stationary culture to the anabiotic state with the formation of cystlike resting cells (CRC), even in non-spore-forming bacteria. AHB participate in the regulation of the phenotypic variability of bacteria. The dynamics of extra-and intracellular concentrations of AHB in growing microbial cultures and the polymodality of their effect determine the adaptogenic functions of AHB as autoinhibitors of culture growth, autoinducers of anabiosis, and autoinhibitors of germination of resting forms. Manifestation of any given function depends on the concentration of AHB, the physiological state of the recipient cells, and on environmental factors. The species nonspecificity of AHB effects points to their significant role in the regulation of the development and functioning of microbial communities.

Adaptogenic functions of extracellular autoregulators of microorganisms

A thermotolerant, Gram-positive, aerobic, endospore-forming, acidophilic bacterium (strain Kr1T) was isolated from the pulp of a gold-containing sulfide concentrate processed at 40 degrees C in a gold-recovery plant (Siberia). Cells of strain Kr1(T) were straight to slightly curved rods, 0.8-1.2 microm in diameter and 1.5-4.5 microm in length. Strain Kr1T formed spherical and oval, refractile, subterminally located endospores. The temperature range for growth was 20-60 degrees C, with an optimum at 40 degrees C. The pH range for growth on medium containing ferrous iron was 1.2-2.4, with an optimum at pH 2.0; the pH range for growth on medium containing S0 was 2.0-5.0, with an optimum at pH 2.5. Strain Kr1T was mixotrophic, oxidizing ferrous iron, S0, tetrathionate or sulfide minerals as energy sources in the presence of 0.02 % yeast extract or other organic substrates. The G+C content of the DNA of strain Kr1T was 48.2+/-0.5 mol%. Strain Kr1T showed a low level of DNA-DNA reassociation with the known Sulfobacillus species (11-44 %). 16S rRNA gene sequence analysis revealed that Kr1T formed a separate phylogenetic group with a high degree of similarity between the nucleotide sequences (98.3-99.6 %) and 100 % bootstrap support within the phylogenetic Sulfobacillus cluster. On the basis of its physiological properties and the results of phylogenetic analyses, strain Kr1T can be affiliated to a novel species of the genus Sulfobacillus, for which the name Sulfobacillus thermotolerans sp. nov. is proposed. The type strain is Kr1T (=VKM B-2339T=DSM 17362T).

N. E. Suzina

Papers

Anoxybacillus pushchinensis gen. nov., sp. nov., a novel anaerobic, alkaliphilic, moderately thermophilic bacterium from manure, and description of Anoxybacillus flavitherms comb. nov.

Dormant forms of Mycobacterium smegmatis with distinct morphology

Adaptogenic functions of extracellular autoregulators of microorganisms

Sulfobacillus thermotolerans sp. nov., a thermotolerant, chemolithotrophic bacterium

New magnet-sensitive structures in bacterial and archaeal cells.