The presence of salt tolerant protease activity has been reported for Halobacterium halobium , Natrialba magadii , and Natronococcus occultus [ 25 — 27 ]. In another study, optimum protease activity of a haloalkaliphilic bacteria S5 isolated from saline habitat of coastal Gujarat, India, was observed at 1. Thus, comparison of the results from our study with the existing literature revealed that protease produced by halophilic bacterial isolates SS1 and SS3 exhibit the best halotolerance, being active up to 1.
Owing to their ability to function in the presence of organic solvents, halophilic lipases are advantageous as lipase mediated catalysis occurs at interface of aqueous and organic layers. Since lipases are advantageous for several applications, the halophilic bacterial isolates of Lunsu were explored for lipase production. SS2 isolate was found to possess extracellular lipase activity. The optimum salt concentration, pH, and temperature for lipase activity of bacterial isolate SS2 were 0.
Moderate halophiles of the genera Bacillus and Staphylococcus isolated from Maharlu salt lake in Iran were reported positive for lipase activity [ 30 ]. Extreme halotolerant lipase was also reported from Haloarcula marismortui [ 31 , 32 ]. A halophilic strain Chromohalobacter sp. LY with high lipolytic activity was isolated from salt lake of Yuncheng, China [ 33 ].
Similarly, halophilic lipase from the halotolerant Staphylococcus warneri PB showed optimum pH of 7. It was stable between pH 7. The purified lipase showed maximum activity in the presence of 2. Thus, the halophilic bacterial isolate SS2 can be exploited for production of halotolerant extracellular lipase.
Glutaminases, in general, exhibit activity in the presence of high concentration of salt. Halophiles can be a valuable source of glutaminase, owing to their production of halozymes. In the present study, halophilic bacterial isolates SS2, SS3, SS5, and SS8 exhibited the ability to secrete extracellular glutaminase with diverse properties.
The glutaminase activity of halophilic bacterial isolates SS2, SS3, SS5, and SS8 was found to be salt tolerant, and the enzyme remained functional in the presence of 2.
Glutaminase from Stenotrophomonas maltophilia NYW was found to be stable in the presence of 2. The marine Micrococcus luteus K3 was reported to have glutaminase activity at pH 8.
Although glutaminase has been studied in fungi and other mesophilic bacteria, very few reports exist on glutaminase from halophiles. In this context, the halophilic bacterial isolates of Lunsu serve as a novel source of glutaminase from the halophilic domain. The cost effective extracellular enzymes produced by halophilic isolates of Lunsu have great economical potential in industrial, agricultural, chemical, pharmaceutical, and biotechnological applications.
The combined hydrolytic activity of some halophilic bacterial isolates can be used for bioconversion of organic materials to useful products in hypersaline or polluted environments.
Owing to their ability to remain functional in extreme conditions such as high temperatures, wide range of pH, and high salt concentrations, the halozymes isolated in this study offer important biotechnological potential. The authors are thankful to Shoolini University, Solan, for the financial and infrastructural support provided for this study. This is an open access article distributed under the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Article of the Year Award: Outstanding research contributions of , as selected by our Chief Editors. Read the winning articles. Journal overview. Special Issues. Received 28 Sep Revised 08 Dec Accepted 16 Dec Published 18 Jan Introduction Hydrolases constitute a class of enzymes widely distributed in nature from bacteria to higher eukaryotes. Materials and Methods The halophilic bacterial strains used in this study were isolated from soil sediment of Lunsu water body, Himachal Pradesh, India [ 13 ].
Characterization of Enzymatic Features of Halophilic Bacteria 2. Quantitative Enzyme Assays 2. Amylase Activity Amylase activity was quantified by Dinitrosalicylic acid DNS method using starch as a substrate [ 16 ]. Protease Activity Protease activity was measured as described by Kuberan et al. Glutaminase Activity The glutaminase enzyme activity was measured by estimating the amount of ammonia liberated from glutamine [ 19 ]. Lipase Activity Lipase assay mixture consisted of 0.
Results 3. Figure 1. Screening and characterization of halophilic bacterial isolates for amylase activity. In each panel, the data represent an average of three independent experiments with standard deviation. Table 1. Biochemical characterization of halozymes. The optimum conditions for the respective enzyme activities are indicated. Figure 2. Screening and characterization of halophilic bacterial isolates for protease activity. Figure 3. Screening and characterization of halophilic bacterial isolates for lipase production.
Figure 4. Screening and characterization of halophilic bacterial isolates for glutaminase production. The change in colour of medium from yellow to pink indicates glutaminase activity. SS8 was plotted against the different concentration of sodium chloride NaCl b , varying pH c , and temperature d as indicated.
Two samples of salted fish from local fish salting factories and two laboratory strains were used. The factory samples were matured anchovy and anchovy fillets in oil, and the laboratory strains were: Haloarcula spp. IRAM and Gibbons were also used enriched with milk. In the SAMm medium, there were obtained count values similar or higher than the ones of the traditional media; besides the simplicity of its elaboration, the possibility to obtain positive results two or three days earlier also added to its benefit.
Consequently, it can be considered an alternative to the media traditionally used for the studied halophilic bacteria. Culture alternative medium for the growth of extreme halophilic bacteria in fish products. Fish are highly perishable and will spoil rapidly if improperly handled. There are several preservation methods to avoid fish spoilage and the growth of pathogenic microorganisms, among them salting is a method that has been used for centuries and in many places around the world such as Asia, Europe, Africa and Latin America HUSS, ; WANG et al.
The simplicity of the salting process, its low production cost and the ease of combining it to other preservation methods, such as marinades, ripening, drying or smoking, has led to its popularity and extensive use FUSELLI et al.
At certain concentrations, salt was found to prevent growth of many microorganisms creating an environment unsuitable for microbial proliferation but some halotolerant or halophilic archaeabacteria microorganisms are not affected by salt SORTE; JAGER, ; BARAT et al. The archaeabacteria represent the third line of descent in the evolution of life.
A microorganism is named halophilic when it needs salt concentration higher than the sea water one for its development. Halophilic bacteria have suffered an adaptative evolutionary process and their physiology was definitively modified to grow and survive in this environment Montero et al. They can be moderate or extreme halophilic bacteria.
Taxonomically, they are included in the Halobacterials order with only one Family, Halobacteriaceae. Ventosa et al. This kind of bacteria is very important in salted foods Felix et al. Since the time of anchovy ripening is long and these bacteria can have proteolytic and lipolytic characteristics, their growth can produce unwished changes; therefore, the determination of halophilic bacteria content is an important matter in salted products CZERNER; YEANNES The extreme halophilic archaeobacteria may be selectively isolated in different media, e.
Besides, it is important to consider that the preparation in laboratory of these media is complex. Ramirez et al. Taking these results into account, considering that CMA medium contains milk in its formulation and that the growth requirements for these bacteria are particularly demanding in terms of nutrients; in this work, it was also considered whether a milk enrichment of the IRAM and Gibbons media would improve their development. The modified medium SAMm was compared to the latter media frequently used in halophilic bacteria culture.
Experiments with the laboratory strains: Haloarcula spp. The aim of this work was to determine the effectiveness of the SAMm medium on bacterial growth, comparing it with the other media used for halophilic bacteria, and considering whether a milk enrichment of the IRAM and Gibbons media would improve their development.
Studies of alternative different media for isolation and counting of extremely halophilic bacteria have been carried out in our laboratory. Two different types of samples of salted fish from local fish salting factories and two different types of laboratory strains were used. The factory samples were of matured anchovy with eight months of ripening time 40 samples and of anchovy fillets in oil 30 samples.
The laboratory strains were: 10 samples of Haloarcula spp. These strains were isolated in laboratory and obtained from salted fish products. The three complex media were alternatively used for the isolation of extremely halophilic bacteria. The cod fish broth basis was prepared with mL of filtered cod fish broth; peptone 1 g; NaCl g. This medium is normally used to observe the proteolytic characteristic in eubacteria.
Thus, taking into account Konig and Steter's proposition, in this work the SAM medium was used with the addition of salts such as MgSO4 and KCl, which improve the development of halophilic microorganisms.
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Leng, N. Bioinformatics 29, — Li, B. Nevertheless, only synthetic wastewater under laboratory conditions was used in this study. Therefore, the investigation of long-term performance using real industrial wastewater would be interesting. Moreover, as salt concentrations were low in this study below 6. To test the robustness of the present approach against contaminations, unsterile industrial wastewater could be used as cultivation medium.
At a smaller scale of ml, a system was developed which used magnetically immobilized Comamonas sp. In parallel, two other reactors were inoculated with Comamonas sp.
JB, one without immobilized cells and the other with nonmagnetically immobilized cells. The wastewater was replaced in the reactors every 12 hr, which corresponds to a sequencing batch mode. Compared to nonimmobilized cells and nonmagnetically immobilized cells, the magnetically immobilized cells showed higher removal rates. The process performance could also be improved, by including electrodes into the bioreactor system for electrical stimulation of the cells.
Besides high removal efficiencies, this systems lacks several factors, which are important for the implementation into industrial process chains. First, the volume of less than one liter is low, which makes scale-up studies necessary. Second, the process was not operated in a continuous mode. Therefore a strategy handling high volume waste streams has to be developed. In contrast, using membranes is a common approach for retaining cells in the bioreactor. The feedforward strategy controls the biomass concentration by adjusting the two parameters 1 glycerol concentration in the feed and 2 the ratio R of cell-free permeate flow F H and the feed flow F F Fig.
The additional carbon source glycerol was used as growth substrate in order to maintain high biomass concentrations and enable high degradation rates of the contaminants. Glycerol is a cheap and widely available carbon source. However, the utilization of other substrates such as acetate or lactate from waste sources is also possible Erian et al.
In terms of scale-up, we reported the construction and utilization of a 21 l corrosion-resistant bubble column bioreactor BCR equipped with a membrane-based cell retention setup Mahler et al. While studying the BCR, we showed the successful cultivation of halophilic cultures in pilot-scale. Compared to the lab-scale bioreactor, the process parameters and yields were similar in the BCR, even though oxygen supply and mixing was provided only through bubbles and not by stirring.
As a result, such a system reduces the operational costs at larger scales and makes the setup easier to maintain. As the experiments were performed under laboratory conditions, it would be interesting to investigate the effect of changing wastewater conditions. Therefore, a long-term cultivation would be interesting, where the composition of the wastewater is altered, in a way that simulates conditions found in a real industrial environment.
Scheme of the cell retention setup. A constant feed F F supplies the cells with fresh substrate and media components. Base F Base is added to hold the pH on a constant level of 7. A pump continuously circulates the cell suspension as loop flow F L through the membrane module to separate cell-free harvest F H. Bleed flow F B is continuously removed to eliminate cells and sustain steady state conditions. Biomass is monitored using a turbidity probe and a soft sensor that is driven by measurements of off-gas composition Mainka et al.
Another study used a forward osmotic hollow fiber filtration unit for cell retention in a continuous bioprocess for the degradation of phenol influent concentration 0. However, the used volume of ml was low and a scale-up to reactor-size should be carried out, in order to investigate potential scale-up effects.
In summary, state-of-the-art bioprocesses for the treatment of saline wastewater, containing aromatic contaminants, deliver good performances according to aromatic degradation efficiencies. Various biological systems were used and different cell retention system could be applied successfully. A comparison of the presented processes can be found in Table 2.
The monitoring of critical process parameters depends on requirements of the wastewater treatment process. Parameters which can be monitored, are physical temperature, pressure, etc. In general, a process monitoring strategy should help to obtain stable and reproducible bioprocesses which meet the desired quality criteria for the treated wastewater Biechele et al.
Although process monitoring is applied to saline and nonsaline processes, saline conditions and an industrial environment cause challenges to the design and usability of sensors and measurement methods.
First of all, the high salt concentrations require materials to withstand the corrosive conditions. Moreover, measurement methods have to overcome interference problems with the salt matrix. The determination of biomass related parameters, like absolute biomass concentration or specific growth rate, is an important topic for bioprocess development, as cells are the biocatalyst Tamburini et al. For instance, in production bioprocesses often a correlation between specific productivity and specific growth rate can be found, thus monitoring the growth rate can help to maintain optimal production parameters Looser et al.
Furthermore, the biomass concentration in wastewater treatment processes is a crucial parameter, not only important for degradation efficiency, but also as the disposal of waste biomass contributes to the operational costs of a wastewater treatment plant Canales et al.
Methods published for the determination and estimation of biomass range from cell count methods on agar plats, to indirect gravimetric determination of cell dry weight to online methods like turbidity measurements and soft sensor estimations Finn et al.
If a dependency between biomass concentration and process performance of bioremediation processes exists, the biomass concentration can be used as control parameter for process optimization. Control parameters need to be available in real-time, thus, data of the biomass concentration have to generated permanently. Thus, microbiological methods like cell count on agar plates or offline methods, such as gravimetric determinations or optical density OD measurements, are not suitable.
Potential alternatives include online methods such as the measurement of turbidity with a turbidity probe, near infrared spectroscopy NIRS , dielectric spectroscopy or mass balancing based on offgas data Finn et al. For using turbidity probes to determine biomass concentration in bioreactors, an a priori calibration with offline biomass data, like the cell dry weight, is needed. Those effects, however, can be avoided by special probe models where samples are passed into a degassed measurement chamber Kiviharju et al.
Also, other suspended solids in the medium e. Therefore, industrial wastewater should be particle free, if accurate turbidity data are needed. A more sophisticated method for the determination of biomass concentration in cell broth would be the use of NIRS-probes. For biomass determination with NIRS-probes, a spectrometer scans wavelength ranges from to 2 nm Finn et al. Information about biomass concentration can, for example, be found in regions from to or to nm Cervera et al.
In order to extract biomass concentration data, it is common to pretreat the absorbance spectra, for example, calculating the second derivative, and build a chemometric model to estimate biomass concentrations Cervera et al. Nevertheless, the NIRS measurements were found to be affected by the aeration rate, the agitation speed, and also the temperature, which has to be considered when building a biomass model Ge et al.
One advantage of NIRS measurement for biomass estimation is the possibility of online ex situ measurements, realized by either flow-through cells or fiber optic process behind a glass wall Cervera et al. Thus, no probes have to be inserted into saline medium containing bioreactors. Moreover, NIRS measurements were also reported for the determination of substrates and products in fermentation broths.
Among those molecules, carbon sources such as glucose, ethanol, glycerol, or lactose were determined, but also ammonia or phosphate were reported to be measured Cervera et al. The monitoring of such metabolites or by-products is important, when the total organic content in the wastewater should be removed.
Also the accumulation of ammonia should be avoided in some cases, for example, for chlor-alkali electrolysis, thus online monitoring of ammonia could be beneficial for process efficiency and security Brinkmann et al.
Alternatively, soft sensors offer the possibility to generate information about biomass concentration by using different process variables. Those variables are measured by several probes and are processed by a software-based algorithm to estimate biomass concentration Biechele et al.
The underlying principles for soft sensors are either model-driven or data-driven. Whereas model-driven soft sensors are based on mass and energy balances, data-driven soft sensors use historical process data for online estimation Biechele et al.
Process variables which are commonly used for biomass soft sensors are offgas values CO 2 , O 2 , base consumption or dissolved oxygen p O 2 Biechele et al.
In comparison to biomass estimation with hard sensors, also soft sensors need offline reference values of biomass concentration to develop and calibrate the underlying models. Nevertheless, soft sensors are able to extend the usability of probes and sensors commonly used for bioprocess and which are often already implemented in existing processes. Therefore, besides the software tools, no investments for additional devices and probes are necessary. Especially for the harsh conditions at treatment plants for industrial saline wastewater, avoiding sensitive probes is beneficial.
Thus, soft sensors for the determination of biomass concentration in saline bioprocesses offer great potential for future process development. This potential could already be shown, as we have recently established a soft sensor for real-time estimation of biomass concentration based on offgas measurements and substrate concentrations in wastewater feeds Mainka et al.
The soft sensor was developed for the extremely halophilic archaeon H. The monitoring of concentrations of specific aromatic compounds like aniline or phenol can be useful, if, for example, thresholds of these compounds in the effluents have to be met. When the wastewater contains more than one aromatic compound, HPLC methods offer the possibility to measure several compounds at once and, depending on the method, with high accuracy.
However, samples have to be taken, either manually or automatically, prepared and the HPLC measurement time considered e. HPLC measurements are time consuming and data are only generated discontinuously. Nevertheless, for purposes, which are uncritical in terms of time like for the comparison of concentrations of wastewater batches with environmental specifications, HPLC methods are suitable and sufficient.
In contrast, if monitoring data are needed for control purposes, data have to be generated in real-time, which can, for example, be realized by sensors.
In literature, several bio sensors and methods for the detection and quantification of aromatic compounds are described Buerck et al.
Online measurement methods for aromatic compounds in wastewater treatment processes need to be highly sensitive and be able to detect also low concentrations. This is true, as the purpose of wastewater treatment plants is the removal of contaminations, and thus, contaminant concentrations should be close to zero. Therefore, the limit of detection of a potential sensor need to be even lower as the threshold, if the concentration of contaminants in a wastewater have to be decreased below a certain threshold.
Otherwise, additional offline measurements are necessary to check the removal efficiency of the process. However, problems occur when aromatics are dissolved in aqueous solutions, as the OH-group of water absorbs strongly at and nm, and thus, overlaps with the CH peaks of aromatics — nm Buerck et al. Prior to determining aromatic concentrations, spectra of pure aromatics were measured and calibration models were generated using partial least squares PLS method.
As this sensor could be promising for monitoring aromatic compounds at wastewater treatment processes, still several things have to be taken into account. The first one is, that concentrations in a mixture of several different aromatics cannot be determined, but a cumulative concentration parameter could be calculated by including data from a filter photometer.
Moreover, the response time of the sensor to concentration changes can range from 2 to more than 20 min, depending on the aromatic species. Also, the sensor has to be implemented inside the bioreactor or a bypass construction, as it has to be in contact with the medium.
Therefore, stability and performance tests for saline wastewater are still necessary. Moreover, potential interferences with cells have to be investigated. In contrast to measure cumulative concentration parameters of aromatics in general, as happened with NIRS measurements, sensors detecting only specific aromatics and being able to differentiate between these compounds have also been reported Maleki et al.
The principles used for the measurement range from optical based systems over enzymatic biosensors to electrochemical detectors. Aromatic compounds which were reported to be measured with sensors are, for example, aniline, catechol, hydroquinone, resorcinol, or 3-methoxyaniline Maleki et al.
Such systems offer the possibility of measuring specific compounds and are suitable for processes where only a small amount of different aromatics are present. However, at microbial degradation processes of aromatics or any other organic contamination, potential intermediates of the degradation pathways could accumulate.
Thus, this accumulation could remain undetected if the sensors can measure the original contaminant but not possible intermediates. Nevertheless, sensors able to measure specific aromatic compounds could be used for quantifying contaminant concentrations in wastewater feeds. Those concentration data could consequently be used for feedforward control strategies, where the bioremediation process is controlled based on composition information of the influent.
An overview of the aromatic bio sensors and their measurement principles is given in Table 3. Those parameters are all measured in different ways.
Therefore, the obtained results offer different possibilities to be interpreted. The long timespan makes this measurement method obviously not suitable for real-time monitoring. However, BOD methods were developed which deliver results with 5—10 min Bourgeois et al. The COD analysis gives information about the oxidation ability of organic compounds in wastewater samples, by using strong oxidizing agents e.
Drawbacks of COD analysis are that biologically inert organic compounds cannot be differentiated from biodegradable content and the generation of hazardous waste e. Simultaneously to organic substances, chloride ions in saline samples react with chromate ions and therefore increase measurement errors Kayaalp et al. In both cases, inorganic carbon needs to be eliminated prior to measure TOC.
Also, both methods have some drawbacks. The high temperature method is sensitive to salts, as salts could produce a melt on the catalytic surface. Those probes use the principle of many organic substances to absorb light at specific wavelengths e. Online spectrometers can detect organic matter in concentration ranges down to ppb, and are widely used in wastewater treatment plants for monitoring and control purposes Van Den Broeke et al.
As the use of online spectrometers only delivers indirect measurement values, a calibration procedure with offline values is required Langergraber et al.
However, suspended solids influence spectroscopic measurements, due to light scattering and shading. Therefore, compensations are necessary to obtain accurate measurements Van Den Broeke et al. In this review, we showed the potential to use halophilic microorganisms for biological treatment of industrial saline wastewater contaminated with aromatic compounds. In that course, we highlighted the need for treating aromatic compounds-containing wastewater, suggested requirements for industrial wastewater processes, gave examples of halophilic bioremediation processes reported in the literature and discussed potential aspects of further research and development topics.
Studies dealing with the degradation of aromatics in saline wastewater showed the proof of principle of using halophiles, as high removal efficiencies for the tested contaminants were reached. Also, reports showed that continuous bioprocesses in lab-scale bioreactor systems including cell retention units are working successfully.
Nevertheless, for the implementation of halophilic bioremediation processes into industrial production environments, several problems still have to be solved or investigated.
Most studies used lab scale systems with a volume well below 20 l. One reason might be the technical effort of large-scale experiments, but also investment costs play an important role. Therefore, experiments in larger scales are necessary to investigate potential scale-up effects. For that reason, collaborations with industrial project partners could intensify the research of large-scale bioremediation processes for saline wastewater.
In particular, the usage of cell retention system in large scales should be examined considering long-term process performance. In addition, wastewater used in scientific studies were mostly synthetic wastewater with only little number of tested contaminants. For addressing the complexity of most industrial wastewater, more studies should be performed using real industrial waste streams.
To do so, industrial collaborations would be again a suitable way to take the research a step further. The industrial implementation of halophilic bioremediation processes also has to solve issues on the level of process technologies.
For instance, corrosion-resistant bioreactor systems are needed when saline wastewater are used, in order to reduce technical problems like leakages in pipes, pumps, or valves.
Furthermore, a complete halophilic bioremediation process necessitates a suitable process monitoring system for critical process parameters like biomass concentration, TOC levels or contaminant concentrations.
Such a system could consist of both, hard and soft sensors. A complete monitoring and control strategy for a bioremediation process of aromatics containing wastewater should consist of different sensor systems.
Online sensors for the measurement of aromatic concentrations in the feed, biomass estimation in the bioreactor based on soft sensors and the measurement of an organic sum parameter e.
Those parameters could then be used as input parameters for a control strategy, which would help to improve and maintain process performance over longer operation periods. Although hard e. Information gathered by specialized sensors can help to improve process understanding, which could result in higher process efficiency. Future research in the field of bioremediation of saline wastewater should also pay attention to environmental regulations concerning maximum levels of contaminants allowed to be released into the environment.
As regulations differ between countries and also depend on the industrial sectors, information about maximum TOC or COD levels allowed for release should already be included during the process design phase. In conclusion, halophilic organisms are promising catalysts for purification of saline, industrial wastewater.
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