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Plant growth-promoting rhizobacteria effect on maize growth and microbial biomass in a chromium-contaminated soil

ABSTRACT

Chromium contamination in soils affects plant growth and this metal can accumulate in plants tissues. In addition, Cr can affect soil microbial biomass and activity. On the other hand, plant growth-promoting rhizobacteria (PGPR) can protect plants against metals and, at the same time, promote plant growth and could alleviate adverse effects on microbial biomass. This study evaluated five PGPR on maize growth, Cr accumulation and soil microbial biomass in a Cr-contaminated soil. Five PGPR (LCC04, LCC41, LCC69, LCC81 and IPA403), isolated from soil under permanent application of composted tannery sludge and contaminated with Cr, were inoculated in maize plants grown in soils with (+Cr) and without (–Cr) Cr. In Cr-contaminated soil, LCC41 promoted the highest growth of maize, while LCC04 contributed with the highest N accumulation. The shoots of maize accumulated less Cr with LCC81, while LCC41 contributed to the highest Cr accumulation in roots. The translocation of Cr was highest with IPA403, while LCC81 contributed to reduce Cr translocation. In conclusion, LCC41 and LCC81 could be effective as PGPR inoculants to promote plant growth and reduce Cr accumulation in maize, respectively, in Cr contaminated soil.

Key words
metals; tannery sludge; soil contamination; PGPR

INTRODUCTION

The accumulation of metals in soils has been an important environmental issue, since these elements are not naturally degraded, persist in the ecosystem and are translocated to different parts of plants (Ogundiran and Osibanjo 2009Ogundiran, M. B., and Osibanjo, O. (2009). Mobility and speciation of heavy metals in soils impacted by hazardous waste. Chemical Speciation & Bioavailability 21, 59-69. https://doi.org/10.3184/095422909X449481
https://doi.org/10.3184/095422909X449481...
). Particularly, chromium (Cr) shows high accumulation in soils, especially on those with a history of application of Cr-contaminated sludge, such as tannery sludge (Araújo et al. 2013Araújo, A. S. F., Silva, M. D. M., Leite, L. F. C., Araujo, F. F., and Dias, N. S. (2013). Soil pH, electric conductivity and organic matter after three years of consecutive amendment of composted tannery sludge. African Journal of Agricultural Research, 8, 1204-1208., 2018Araújo, A. S. F., Santos, V. M., Miranda, A. R. L., Nunes, L. A. P. L., Dias, C. T. S., and Melo W. J. (2018). Chemical variables influencing microbial properties in composted tannery sludge-treated soil. International Journal of Environmental Science and Technology, 15, 1793-1800. https://doi.org/10.1007/s13762-017-1547-0
https://doi.org/10.1007/s13762-017-1547-...
).

Indeed, the long-term application of Cr-contaminated tannery sludge has increased the accumulation of Cr in soils and promoted changes in soil chemical (Araújo et al. 2013Araújo, A. S. F., Silva, M. D. M., Leite, L. F. C., Araujo, F. F., and Dias, N. S. (2013). Soil pH, electric conductivity and organic matter after three years of consecutive amendment of composted tannery sludge. African Journal of Agricultural Research, 8, 1204-1208.), physical (Araújo et al. 2016Araújo, A. S. F., Lima, L. M., Melo, W. J., Santos, V. M., and Araújo, F. F. (2016). Soil properties and cowpea yield after six years of consecutive amendment of composted tannery sludge. Acta Scientiarum Agronomy, 38, 407-413. https://doi.org/10.4025/actasciagron.v38i3.28281
https://doi.org/10.4025/actasciagron.v38...
) and biological properties (Sousa et al. 2017Sousa, R. S., Santos, V. M., Melo, W. J., Nunes, L. A. P. L., Van den Brink, P. J., and Araújo, A. S. F. (2017). Time-dependent effect of composted tannery sludge on the chemical and microbial properties of soil. Ecotoxicology, 26, 1366-1377. https://doi.org/10.1007/s10646-017-1861-9
https://doi.org/10.1007/s10646-017-1861-...
). In addition, Cr accumulated in soil is translocated and bioaccumulated in plants (Sousa et al. 2018Sousa, R. S., Nunes, L. A. P. L., Lima, A. B, Melo, W. J., Antunes, J. E. L., and Araujo, A. S. F. (2018). Chromium accumulation in maize and cowpea after successive applications of composted tannery sludge. Acta Scientiarum Agronomy, 40, e35361. https://doi.org/10.4025/actasciagron.v40i1.35361
https://doi.org/10.4025/actasciagron.v40...
). On the other hand, some studies have found different microbes that showed tolerance to high Cr concentration (Miranda et al. 2018Miranda, A. R. L., Antunes, J. E. L., Araujo, F. F., Melo, V. M. M., Bezerra, W. M., Van den Brink, P. J., and Araújo, A. S. F. (2018). Less abundant bacterial groups are more affected than the most abundant groups in composted tannery sludge-treated soil. Scientific Reports, 8, 11755. https://doi.org/10.1038/s41598-018-30292-1
https://doi.org/10.1038/s41598-018-30292...
, 2019Miranda, A. R. L., Mendes, L. W., Lemos, L. N., Antunes, J. E. L., Amorim, M. R., Melo, V. M. M., Melo, W. J., Van den Brink, P. J., and Araújo, A. S. F. (2019). Dynamics of archaeal community in soil with application of composted tannery sludge. Scientific Reports, 9, 7347. https://doi.org/10.1038/s41598-019-43478-y
https://doi.org/10.1038/s41598-019-43478...
), including plant growth-promoting rhizobacteria (PGPR) (Rocha et al. 2019Rocha, S. M. B., Antunes, J. E. L., Araujo, J. M. A., Aquino, J. P. A., Melo, W. J., Mendes, L. W., and Araújo, A. S. F. (2019). Capability of plant growth-promoting bacteria in chromium-contaminated soil after application of composted tannery sludge. Annals of Microbiology, 69, 665-671. https://doi.org/10.1007/s13213-019-01455-w
https://doi.org/10.1007/s13213-019-01455...
).

Some PGPR have been recognized to be tolerant to metal-contaminated soils, since they present different strategies to withstand these elements (Hao et al. 2014Hao, X., Taghavi, S., Xie, P., Orbach, M. J., Alwathnani, H. A., Rensing, C., and Wei, G. (2014). Phytoremediation of heavy and transition metals aided by legume-rhizobia symbiosis. International Journal of Phytoremediation, 6, 179-202. https://doi.org/10.1080/15226514.2013.773273
https://doi.org/10.1080/15226514.2013.77...
; Ojuederie and Babalola 2017Ojuederie, O. B., and Babalola, O. O. (2017). Microbial and plant-assisted bioremediation of heavy metal polluted environments: A review. International Journal of Environmental Research and Public Health, 14, 1504. https://doi.org/10.3390/ijerph14121504
https://doi.org/10.3390/ijerph14121504...
). Some strategies include the secretion of enzymes and bioactive metabolites that could protect plants against metals and, at the same time, promoting plant growth (Hao et al. 2014Hao, X., Taghavi, S., Xie, P., Orbach, M. J., Alwathnani, H. A., Rensing, C., and Wei, G. (2014). Phytoremediation of heavy and transition metals aided by legume-rhizobia symbiosis. International Journal of Phytoremediation, 6, 179-202. https://doi.org/10.1080/15226514.2013.773273
https://doi.org/10.1080/15226514.2013.77...
). For instance, PGPR produce and release enzymes and exopolysaccharide (EPS) that can assist in metal detoxification and, indirectly, improve plant growth (Lal et al. 2018Lal, S., Ratna, S., Said, O. B., and Kumar, R. (2018). Biosurfactant and exopolysaccharide-assisted rhizobacterial technique for the remediation of heavy metal contaminated soil: An advancement in metal phytoremediation technology. Environmental Technology & Innovation, 10, 243-263. https://doi.org/10.1016/j.eti.2018.02.011
https://doi.org/10.1016/j.eti.2018.02.01...
).

The PGPR tolerance to Cr contamination could be associated with their ability to produce and release enzymes that enable them to thrive under high Cr concentrations (Tirry et al. 2018Tirry, N., Joutey, N. T., Sayel, H., Kouchou, A., Bahafid, W., Asri, M., and El Ghachtouli, N. (2018). Screening of plant growth promoting traits in heavy metals resistant bacteria: Prospects in phytoremediation. Journal of Genetic Engineering and Biotechnology, 16, 613-619. https://doi.org/10.1016/j.jgeb.2018.06.004
https://doi.org/10.1016/j.jgeb.2018.06.0...
). In a previous study in a Cr-contaminated soil, Rocha et al. (2019)Rocha, S. M. B., Antunes, J. E. L., Araujo, J. M. A., Aquino, J. P. A., Melo, W. J., Mendes, L. W., and Araújo, A. S. F. (2019). Capability of plant growth-promoting bacteria in chromium-contaminated soil after application of composted tannery sludge. Annals of Microbiology, 69, 665-671. https://doi.org/10.1007/s13213-019-01455-w
https://doi.org/10.1007/s13213-019-01455...
selected some PGPR with high biochemical capability, i.e., urease, catalase and phosphate solubilization activity, and tolerance to high Cr concentrations. Therefore, the use of these Cr-tolerant PGPR may present potential in Cr-contaminated soil by acting on plant growth promotion (Anyanwu and Ezaka 2011Anyanwu, C. U., and Ezaka, E. (2011). Growth Responses of Chromium (vi) Tolerant Bacteria to Different Concentrations of Chromium. International Journal of Basic and Applied Science, 11, 41-44.). Plant growth-promoting rhizobacteria could also alleviate the effect of Cr on soil microbial biomass and activity by stimulating root growth and enhancing the rhizosphere effect (Souza et al. 2015Souza, R., Ambrosini, A., and Passaglia, L. M. P. (2015). Plant growth-promoting bacteria as inoculants in agricultural soils. Genetics and Molecular Biology, 38, 401-419.). In addition, the production of extracellular enzymes by PGPR contributes to decompose organic residues and increase microbial biomass and activity (Moraes et al. 2018Moraes, M. C. H. S., Medeiros, E. V., Andrade, D. S., Lima, L. D., Santos, I. C. S., and Martins Filho, A. P. (2018). Microbial biomass and enzymatic activities in sandy soil cultivated with lettuce inoculated with plant growth promoters. Revista Caatinga, 31, 860-870. https://doi.org/10.1590/1983-21252018v31n408rc
https://doi.org/10.1590/1983-21252018v31...
).

The hypothesis of this study is that the inoculation of selected PGPR could stimulate plant growth and improve soil microbial biomass in Cr-contaminated soils. Therefore, five potential PGPR, that present high biochemical capability, Cr tolerance and production of EPS (Rocha et al. 2019Rocha, S. M. B., Antunes, J. E. L., Araujo, J. M. A., Aquino, J. P. A., Melo, W. J., Mendes, L. W., and Araújo, A. S. F. (2019). Capability of plant growth-promoting bacteria in chromium-contaminated soil after application of composted tannery sludge. Annals of Microbiology, 69, 665-671. https://doi.org/10.1007/s13213-019-01455-w
https://doi.org/10.1007/s13213-019-01455...
) were evaluated in a pot experiment. The features presented by these PGPR could contribute to ameliorate Cr stress, avoid Cr translocation on plants and promote plant growth. Thus, the aim of this study was to evaluate the inoculation effect of five PGPR on maize growth and microbial biomass in both noncontaminated and Cr-contaminated soil.

MATERIAL AND METHODS

The study was conducted in a greenhouse located at the Department of Soil and Agricultural Engineering (DEAS), Federal University of Piauí, Brazil (05°05’S, 42°48’W; 75 m). Pots (2.8 L) were filled with soil (Fluvic Neosol) collected from a long-term experimental field with a history of application of composted tannery sludge (CTS). In this study, soil samples were collected from plots with application of 20 ton·ha–1 CTS (highest rate). This soil presents an accumulation of about 300 mg·kg–1 Cr. As a control without CTS, soil samples were collected from an adjacent site (without CTS application) that does not present Cr.

The Cr was extracted from the soil by the DTPA-TEA method and measured using the USEPA-3050 method (EPA 1986[EPA] United States Environmental Protection Agency. (1986). Test Methods for Evaluating Solid Waste: Volume IA - Laboratory Manual, Physical/Chemical Methods. Washington: EPA.). Thus, two soil conditions were used in this experiment, according to Cr concentration: soil without Cr (–Cr) and soil with Cr (+Cr). Soil chemical analysis were conducted using air dried and sieved (2 mm) samples. Soil pH, exchangeable Ca2+, Mg2+, K+, and the available P were estimated according to EMBRAPA (1997)[EMBRAPA] Empresa Brasileira de Pesquisa Agropecuária. (1997) Centro Nacional de Pesquisa de Solos. Serviço nacional de levantamento e conservação do solo. Manual de métodos de análise de solo. Rio de Janeiro: Embrapa Solos, 212p.. Soil organic C (TOC) was determined by wet combustion using a mixture of 5 mL of 0.167 mol·L–1 potassium dichromate and 7.5 mL of concentrated sulfuric acid under heating (170 °C for 30 min) (Yeomans and Bremner 1988Yeomans, J. C., and Bremner, J. M. A rapid and precise method for routine determination of organic carbon in soil. Communication in Soil Science and Plant Analysis, 19:1467-1476, 1988. https://doi.org/10.1080/00103628809368027
https://doi.org/10.1080/0010362880936802...
). The chemical characteristics of the soils are shown in Table 1.

Table 1
Chemical characteristics of soils.

This study evaluated four potential PGPR that presented high biochemical capability (urease, catalase and phosphate solubilization activity), tolerance to Cr and production of EPS (Rocha et al. 2019Rocha, S. M. B., Antunes, J. E. L., Araujo, J. M. A., Aquino, J. P. A., Melo, W. J., Mendes, L. W., and Araújo, A. S. F. (2019). Capability of plant growth-promoting bacteria in chromium-contaminated soil after application of composted tannery sludge. Annals of Microbiology, 69, 665-671. https://doi.org/10.1007/s13213-019-01455-w
https://doi.org/10.1007/s13213-019-01455...
) in the presence of Cr, being: LCC04, LCC41, LCC69 and LCC81. A description on the origin of these PGPR is provided by Rocha et al. (2019)Rocha, S. M. B., Antunes, J. E. L., Araujo, J. M. A., Aquino, J. P. A., Melo, W. J., Mendes, L. W., and Araújo, A. S. F. (2019). Capability of plant growth-promoting bacteria in chromium-contaminated soil after application of composted tannery sludge. Annals of Microbiology, 69, 665-671. https://doi.org/10.1007/s13213-019-01455-w
https://doi.org/10.1007/s13213-019-01455...
. Another potential PGPR (IPA403), with high production of EPS (Antunes et al. 2017Antunes, J. E. L., Lyra, M. C. C. P., Ollero, F. J., Freitas, A. D. S., Oliveira, L. M. S., Araújo, A. S. F., and Figueiredo, M. V. B. (2017). Diversity of plant growth-promoting bacteria associated with sugarcane. Genetics and Molecular Research, 16, gmr16029662. https://doi.org/10.4238/gmr16029662
https://doi.org/10.4238/gmr16029662...
) was also evaluated. A treatment without inoculation was used as control. The experiment design was completely randomized in a factorial scheme with two Cr concentrations (0 and 300 mg·kg–1) and six treatments (LCC04, LCC41, LCC69, LCC81, IPA403 and control), in four replicates.

All rhizobacteria were grown in nutrient agar solid medium containing 3.0 g·L–1 of yeast extract, 5 g·L–1 of peptone and 20 g·L–1 of agar for 48 h at 32 °C. Bacterial colonies were transferred to 100 mL of sterile saline water supplied with 0.01 mol·mL–1 MgSO4 and the suspension was stirred in vortex for bacterial dispersion. Bacterial inoculant concentration was adjusted to 1.0 × 108 cells·mL–1. These aqueous suspensions containing each isolate were used as bacterial inoculants. Maize (Zea mays L., AG1061) seeds were surface-disinfested (5% sodium hypochlorite for 3 min) and rinsed with sterile distilled water. These disinfested seeds were used in the experimental procedures. The bacterial aqueous suspension was applied directly onto the seeds during planting in the amount of 1 mL per seed. Eight days after germination, plants were thinned, leaving one plant per pot. Each pot received 600 mg ammonium sulphate, 410 mg super single phosphate and 225 mg potassium chloride. The rates of ammonium sulphate and potassium chloride were divided into two applications (at 15 and 40 days after emergence). Pots were irrigated daily with sterilized water to maintain soil moisture at 70% of field capacity.

At harvest (60 days after plant emergence at pre-flowering stage), soil and plants were collected. Soil microbial biomass C (MBC) was estimated using the chloroform fumigation-extraction method according to Vance et al. (1987)Vance, E. D., Brookes, P. C., and Jenkinson, D.S. (1987). An extraction method for measuring soil microbial biomass C. Soil Biology and Biochemistry, 19, 703-707. https://doi.org/10.1016/0038-0717(87)90052-6
https://doi.org/10.1016/0038-0717(87)900...
. The extraction efficiency coefficients of 0.38 was used to convert the difference in C between fumigated and nonfumigated soils in MBC. Soil respiration was monitored with a daily measurement of CO2 evolution under aerobic incubation at 25 °C for 7 days (Alef and Nannipieri 1995Alef, K., and Nannipieri, P. (1995). Methods in Applied Soil Microbiology and Biochemistry. New York: Academic Press. https://doi.org/10.1016/B978-012513840-6/50014-8
https://doi.org/10.1016/B978-012513840-6...
). The respiratory quotient (qCO2) was calculated from the ratio between respiration and MBC and is expressed as mg CO2·kg–1·MBC·day–1.

The shoot was separated from roots and they were dried (65 °C; 72 h) and weighed to determine both shoot (SDW) and roots (RDW) dry weight. Total N content in the shoots was estimated by Kjedahl method. The chlorophyll was estimated by a portable chlorophyll meter (Falker ClorofiLOG CFL 1030), according to manufacturer’s instruction (Falker 2008Falker (2008). Automação agrícola. Manual do medidor eletrônico de teor clorofila (ClorofiLOG/CFL 1030). Porto Alegre. 33p. [Accessed Ago. 28, 2019]. Available at: http://www.falker.com.br/produto_download.php?id=4
http://www.falker.com.br/produto_downloa...
). The accumulation of N (AcN) in the shoot was estimated by the SDW and total N content. Chromium content in shoot and roots were estimated according to the method described in USEPA-3050 (EPA 1986[EPA] United States Environmental Protection Agency. (1986). Test Methods for Evaluating Solid Waste: Volume IA - Laboratory Manual, Physical/Chemical Methods. Washington: EPA.). The translocation factor of Cr (TF) (Patel et al. 2016Patel, A., Pandey, V., and Patra, D. D. (2016). Metal absorption properties of Mentha spicata grown under tannery sludge amended soil-its effect on antioxidant system and oil quality. Chemosphere, 147, 67-73. https://doi.org/10.1016/j.chemosphere.2015.12.097
https://doi.org/10.1016/j.chemosphere.20...
) was calculated as Eq. 2:

T F = C r   content in the shoot   ( m g k g 1 ) / C r   content in the roots   ( m g k g 1 ) (2)

TF = Cr content in the shoot (mg·kg–1)/Cr content in the roots (mg·kg–1)(2)

Shapiro–Wilk and Bartlett tests were used to test the normality and homogeneity of variance of data, respectively. Except for Cr accumulation and TF, all data were statistically analyzed using an analysis of variance (ANOVA) considering a factorial design with two soil conditions (–Cr and +Cr) and six treatments (isolates and control), and their interactions. The means were compared by Tukey’s test. All data were analyzed using the R software (R Core Team 2014R Core Team (2014). R: A language and environment for statistical computing. [Accessed Mar. 20, 2021]. Available at: http://www.r-project.org/
http://www.r-project.org/...
).

RESULTS AND DISCUSSION

The results showed differences between the responses to PGPR and soil conditions for all evaluated parameters. In noncontaminated soil, inoculation with LCC81 and LCC41 promoted the highest SDW, while in Cr-contaminated soil, LCC69 contributed to increased SDW (Fig. 1a). The PGPR showed no significant effects with respect to RDW, compared to the control, in noncontaminated soils; however, LCC41 showed a greater RDW than LCC81 (Fig. 1b). In Cr-contaminated soil, inoculation with LCC41 increased RDW as compared with LCC04, LCC81, IPA403 and the control. Inoculation with LCC41 and LCC81 contributed to the highest root:shoot ratio in Cr-contaminated soil (Fig. 1c). In noncontaminated soil, there were no differences between treatments to root:shoot ratio, except the treatment with LCC81, which showed the lowest value.

The results showed that, in Cr-contaminated soil, shoot biomass was significantly stimulated by inoculation with LCC04, LCC41 and LCC69, with a range of 50 to 100%, as compared to the uninoculated control. Previous studies have also reported some Cr-tolerant PGPR increasing the growth of sorghum (Bruno et al. 2020Bruno, L. B., Karthik, C., Ma, Y., Kadirvelu, K., Freitas, H., and Rajkumar, M. (2020). Amelioration of chromium and heat stresses in Sorghum bicolor by Cr6+ reducing-thermotolerant plant growth promoting bacteria. Chemosphere, 244, 125521. https://doi.org/10.1016/j.chemosphere.2019.125521
https://doi.org/10.1016/j.chemosphere.20...
), wheat (Khan et al., 2013Khan, M. Y., Asghar, H. N., Jamshaid, M. U., Akhtar, M. J., and Zahir, Z. A. (2013). Effect of microbial inoculation on wheat growth and phytostabilization of chromium contaminated soil. Pakistan Journal of Botany, 45, 27-34.) and alfalfa (Tirry et al. 2018Tirry, N., Joutey, N. T., Sayel, H., Kouchou, A., Bahafid, W., Asri, M., and El Ghachtouli, N. (2018). Screening of plant growth promoting traits in heavy metals resistant bacteria: Prospects in phytoremediation. Journal of Genetic Engineering and Biotechnology, 16, 613-619. https://doi.org/10.1016/j.jgeb.2018.06.004
https://doi.org/10.1016/j.jgeb.2018.06.0...
) in Cr-contaminated soils.

Plant growth-promoting rhizobacteria present the ability to stimulate plant growth directly, by production of phytohormones, and indirectly, by amelioration of metal stress (Mallick et al. 2018Mallick, I., Bhattacharyya, C., Mukherji, S., Dey, D., Sarkar, S. C., Mukhopadhyay, U. K., and Ghosh, A. (2018). Effective rhizoinoculation and biofilm formation by arsenic immobilizing halophilic plant growth promoting bacteria (PGPB) isolated from mangrove rhizosphere: A step towards arsenic rhizoremediation. Science of The Total Environment, 610-611, 1239-1250. https://doi.org/10.1016/j.scitotenv.2017.07.234
https://doi.org/10.1016/j.scitotenv.2017...
). According to Chiboub et al. (2016)Chiboub, M., Saadani, O., Fatnassi, I. C., Abdelkrim, S., Abid, G., Jebara, M., and Jebara, S. H. (2016). Characterization of efficient plant-growth-promoting bacteria isolated from Sulla coronaria resistant to cadmium and to other heavy metals. Comptes Rendus Biologies, 339, 391-398. https://doi.org/10.1016/j.crvi.2016.04.015
https://doi.org/10.1016/j.crvi.2016.04.0...
, several metal-tolerant PGPR are capable of producing phytohormones, such as indole-3-acetic acid (IAA), and enzymes even under metal stress conditions. Indeed, the selected PGPR used in this study presents high capability of producing IAA and enzymes in Cr-contaminated soils (Rocha et al. 2019Rocha, S. M. B., Antunes, J. E. L., Araujo, J. M. A., Aquino, J. P. A., Melo, W. J., Mendes, L. W., and Araújo, A. S. F. (2019). Capability of plant growth-promoting bacteria in chromium-contaminated soil after application of composted tannery sludge. Annals of Microbiology, 69, 665-671. https://doi.org/10.1007/s13213-019-01455-w
https://doi.org/10.1007/s13213-019-01455...
). Particularly, Rocha et al. (2019)Rocha, S. M. B., Antunes, J. E. L., Araujo, J. M. A., Aquino, J. P. A., Melo, W. J., Mendes, L. W., and Araújo, A. S. F. (2019). Capability of plant growth-promoting bacteria in chromium-contaminated soil after application of composted tannery sludge. Annals of Microbiology, 69, 665-671. https://doi.org/10.1007/s13213-019-01455-w
https://doi.org/10.1007/s13213-019-01455...
found that LCC04, LCC41 and LCC69 presented positive activity of catalase, urease, lipase and phosphate solubilization in Cr-contaminated soil. Thus, the inoculation with these isolates contributed to increased maize growth in Cr-contaminated soil. In noncontaminated soil, inoculation with LCC81 increased maize shoot growth, although this response was not observed in Cr-contaminated soil.

Figure 1
Shoot (a) and roots (b) dry weight, and root:shoot ratio (c) of maize inoculated with PGPR grown in soil with (+Cr) and without (–Cr) Cr.

In regard to root growth, LCC41 promoted about three times greater root biomass than uninoculated plants. In a previous study, LCC41 was found to be a high producer of IAA in Cr-contaminated soil (70 μg IAA·mL–1 in soil under 100 mg Cr·kg–1; Rocha et al. 2019Rocha, S. M. B., Antunes, J. E. L., Araujo, J. M. A., Aquino, J. P. A., Melo, W. J., Mendes, L. W., and Araújo, A. S. F. (2019). Capability of plant growth-promoting bacteria in chromium-contaminated soil after application of composted tannery sludge. Annals of Microbiology, 69, 665-671. https://doi.org/10.1007/s13213-019-01455-w
https://doi.org/10.1007/s13213-019-01455...
). Indole-3-acetic acid is the most common plant hormone of the auxin class, being required for root development (Tian et al. 2014Tian, H., De Smet, I., and Ding, Z. (2014). Shaping a root system: regulating lateral versus primary root growth. Trends in Plant Science, 19, 426-431. https://doi.org/10.1016/j.tplants.2014.01.007
https://doi.org/10.1016/j.tplants.2014.0...
). Thus, the increased root growth with LCC41 was likely influenced by its high capability in producing IAA. Since LCC41 stimulated more root growth in Cr-contaminated soil, it contributed to the highest root:shoot ratio found in this treatment. The higher root:shoot ratio found with LCC41 suggests that this isolate could ameliorate possible negative effects of Cr on root growth.

Under both soil conditions, maize accumulated more N with the inoculation of LCC04 (Fig. 2a). The LCC04 also contributed to the highest values of chlorophyll in noncontaminated soil (Fig. 2b), while in Cr-contaminated soil no significant differences were observed between treatments. These results suggest that LCC04 is able to contribute N to plants under both soil conditions. Since this PGPR was isolated from Cr-contaminated soil (Rocha et al. 2019Rocha, S. M. B., Antunes, J. E. L., Araujo, J. M. A., Aquino, J. P. A., Melo, W. J., Mendes, L. W., and Araújo, A. S. F. (2019). Capability of plant growth-promoting bacteria in chromium-contaminated soil after application of composted tannery sludge. Annals of Microbiology, 69, 665-671. https://doi.org/10.1007/s13213-019-01455-w
https://doi.org/10.1007/s13213-019-01455...
), it may have been conferred the ability to fix or contribute N even under Cr stress. Therefore, the higher N accumulation observed in plants by inoculation with LCC04 reflects its Cr-tolerance and biochemical capability in Cr-contaminated soils. Compared to other PGPR, LCC04 is catalase, urease and phosphatase positive in soil with 200 mg Cr·kg–1 (Rocha et al. 2019Rocha, S. M. B., Antunes, J. E. L., Araujo, J. M. A., Aquino, J. P. A., Melo, W. J., Mendes, L. W., and Araújo, A. S. F. (2019). Capability of plant growth-promoting bacteria in chromium-contaminated soil after application of composted tannery sludge. Annals of Microbiology, 69, 665-671. https://doi.org/10.1007/s13213-019-01455-w
https://doi.org/10.1007/s13213-019-01455...
). The urease catalyzes the hydrolysis of urea to ammonium and then it can be absorbed by plants (Nosheen and Bano 2014Nosheen, A., and Bano, A. (2014). Potential of plant growth promoting rhizobacteria and chemical fertilizers on soil enzymes and plant growth. Pakistan Journal of Botany, 46, 1521-1530.), while catalase protects plants against oxidative stress (Santos et al. 2018Santos, A. A., Silveira, J. A. G., Bonifacio, A., Rodrigues, A. C., and Figueiredo, M. V. B. (2018). Antioxidant response of cowpea co-inoculated with plant growth-promoting bacteria under salt stress. Brazilian Journal of Microbiology, 49, 513-521. https://doi.org/10.1016/j.bjm.2017.12.003
https://doi.org/10.1016/j.bjm.2017.12.00...
). Consequently, the higher N accumulation in plants, by inoculating with LCC04, increased chlorophyll content. Chlorophyll is a pigment related to photosynthesis, being important to confer plant growth (Kanwal et al. 2017Kanwal, S., Ilyas, N., Batool, N., and Arshad, M. (2017). Amelioration of drought stress in wheat by combined application of PGPR, compost, and mineral fertilizer. Journal of Plant Nutrition, 40, 1250-1260. https://doi.org/10.1080/01904167.2016.1263322
https://doi.org/10.1080/01904167.2016.12...
) and some studies have reported PGPR increasing chlorophyll content in maize (Kifle and Laing 2016Kifle, M. H., and Laing, M. D. (2016). Isolation and screening of bacteria for their diazotrophic potential and their influence on growth promotion of maize seedlings in greenhouses. Frontiers in Plant Science, 6, 1225. https://doi.org/10.3389/fpls.2015.01225
https://doi.org/10.3389/fpls.2015.01225...
; Aquino et al. 2019Aquino, J. P. A., Macedo Junior, F. B., Antunes, J. E. L., Figueiredo, M. V. B., Alcântara Neto, F., Araujo, A. S. F. (2019). Plant growth-promoting endophytic bacteria on maize and sorghum. Pesquisa Agropecuária Tropical, 49, e56241. https://doi.org/10.1590/1983-40632019v4956241
https://doi.org/10.1590/1983-40632019v49...
). Interestingly, IPA403 is an isolate with efficiency to contribute N to maize, but it was isolated from a noncontaminated soil by Antunes et al. (2017)Antunes, J. E. L., Lyra, M. C. C. P., Ollero, F. J., Freitas, A. D. S., Oliveira, L. M. S., Araújo, A. S. F., and Figueiredo, M. V. B. (2017). Diversity of plant growth-promoting bacteria associated with sugarcane. Genetics and Molecular Research, 16, gmr16029662. https://doi.org/10.4238/gmr16029662
https://doi.org/10.4238/gmr16029662...
. Thus, IPA403 was apparently not able to contribute N in the Cr-contaminated soil.

Figure 2
Nitrogen (a) and chlorophyll (b) content in maize leaves inoculated with PGPB grown in soil with (+Cr) and without (–Cr) Cr.

The accumulation of Cr was more pronounced in roots than in shoots (Fig. 3a). In Cr-contaminated soil, the shoots accumulated less Cr with inoculation with LCC81. In contrast, plants inoculated with IPA403 and those not inoculated accumulated more Cr in shoot. Roots accumulated more Cr in plants inoculated with LCC41. The inoculation with IPA403 and LCC81 contributed to the highest and lowest TF, respectively (Fig. 3b).

Figure 3
Chromium accumulation in plants (a) and the translocation factor (b) in maize inoculated with PGPB grown in soil with (+Cr) and without (–Cr) Cr.

The higher accumulation of Cr, in roots than shoots, agrees with previous studies that have shown metals being preferentially accumulated in maize roots, such as Cr (Sousa et al. 2018Sousa, R. S., Nunes, L. A. P. L., Lima, A. B, Melo, W. J., Antunes, J. E. L., and Araujo, A. S. F. (2018). Chromium accumulation in maize and cowpea after successive applications of composted tannery sludge. Acta Scientiarum Agronomy, 40, e35361. https://doi.org/10.4025/actasciagron.v40i1.35361
https://doi.org/10.4025/actasciagron.v40...
) and Cu (Rizvi and Khan 2018Rizvi, A., and Khan, M. S. (2018). Heavy metal induced oxidative damage and root morphology alterations of maize (Zea mays L.) plants and stress mitigation by metal tolerant nitrogen fixing Azotobacter chroococcum. Ecotoxicology and Environmental Safety, 157, 9-20. https://doi.org/10.1016/j.ecoenv.2018.03.063
https://doi.org/10.1016/j.ecoenv.2018.03...
). Recently, Sousa et al. (2018)Sousa, R. S., Nunes, L. A. P. L., Lima, A. B, Melo, W. J., Antunes, J. E. L., and Araujo, A. S. F. (2018). Chromium accumulation in maize and cowpea after successive applications of composted tannery sludge. Acta Scientiarum Agronomy, 40, e35361. https://doi.org/10.4025/actasciagron.v40i1.35361
https://doi.org/10.4025/actasciagron.v40...
assessed the accumulation of Cr in maize and cowpea and found higher accumulation in roots. The results showed roots accumulating more Cr when inoculated with LCC41 and could be related to the higher root growth and root:shoot ratio found in this treatment.

In Cr-contaminated soil, the inoculation with LCC81 reduced the translocation of Cr from roots to shoot. Recent studies have reported that metal-tolerant PGPR could present the ability to immobilize and reduce the bioavailability of metals and their consequent accumulation in plants and, at the same time, promote plant growth (Han et al. 2018Han, H., Sheng, X., Hu, J., He, L., and Wang, Q. (2018). Metal-immobilizing Serratia liquefaciens CL-1 and Bacillus thuringiensis X30 increase biomass and reduce heavy metal accumulation of radish under field conditions. Ecotoxicology and Environmental Safety, 161, 526-533. https://doi.org/10.1016/j.ecoenv.2018.06.033
https://doi.org/10.1016/j.ecoenv.2018.06...
; Wang et al. 2018Wang, Q., Zhang, W.-J., He, L.-Y., and Sheng, X.-F. (2018). Increased biomass and quality and reduced heavy metal accumulation of edible tissues of vegetables in the presence of Cd-tolerant and immobilizing Bacillus megaterium H3. Ecotoxicology and Environmental Safety, 148, 269-274. https://doi.org/10.1016/j.ecoenv.2017.10.036
https://doi.org/10.1016/j.ecoenv.2017.10...
). For instance, Bacillus megaterium promoted the growth of Brassica juncea, Luffa cylindrica and Sorghum halepense and contributed to decrease the translocation of Ni from roots to shoots (Rajkumar et al. 2013Rajkumar, M., Ma, Y., and Freitas, H. (2013). Improvement of Ni phytostabilization by inoculation of Ni resistant Bacillus megaterium SR28C. Journal of Environmental Management, 128, 973-980. https://doi.org/10.1016/j.jenvman.2013.07.001
https://doi.org/10.1016/j.jenvman.2013.0...
). Recently, Rizvi and Khan (2018)Rizvi, A., and Khan, M. S. (2018). Heavy metal induced oxidative damage and root morphology alterations of maize (Zea mays L.) plants and stress mitigation by metal tolerant nitrogen fixing Azotobacter chroococcum. Ecotoxicology and Environmental Safety, 157, 9-20. https://doi.org/10.1016/j.ecoenv.2018.03.063
https://doi.org/10.1016/j.ecoenv.2018.03...
reported that inoculation with Azotobacter chroococcum lowered the Cu and Pb accumulation in maize and that this was due to metal chelation and immobilization. There is some speculation that some substances produced by PGPR, such as IAA, siderophores and EPS, could help plants to resist metal contamination. In addition, these PGPR also were shown to form biofilms, which restricted metal uptake in these plants (Das and Sarkar 2018Das, J., and Sarkar, P. (2018). Remediation of arsenic in mung bean (Vigna radiata) with growth enhancement by unique arsenic-resistant bacterium Acinetobacter lwoffii. Science of The Total Environment, 624, 1106-1118. https://doi.org/10.1016/j.scitotenv.2017.12.157
https://doi.org/10.1016/j.scitotenv.2017...
; Rizvi and Khan 2018Rizvi, A., and Khan, M. S. (2018). Heavy metal induced oxidative damage and root morphology alterations of maize (Zea mays L.) plants and stress mitigation by metal tolerant nitrogen fixing Azotobacter chroococcum. Ecotoxicology and Environmental Safety, 157, 9-20. https://doi.org/10.1016/j.ecoenv.2018.03.063
https://doi.org/10.1016/j.ecoenv.2018.03...
).

The inoculation with LCC41 increased soil respiration in both noncontaminated and Cr-contaminated soils (Fig. 4a). LCC69 also contributed to increase soil respiration in Cr-contaminated soil. In noncontaminated and Cr-contaminated soils, LCC04 and IPA403 decreased soil respiration, respectively. Microbial biomass C was higher in both noncontaminated and Cr-contaminated soils with LCC69 inoculation (Fig. 4b). LCC04 and LCC81 also contributed to high MBC in Cr-contaminated soil. The lowest values of MBC in both soil conditions were found in the uninoculated soil. In noncontaminated soil, qCO2 was higher and lower with the inoculation of LCC41 and uninoculated soil, respectively (Fig. 4c). In contrast, uninoculated soil had the highest qCO2 in Cr-contaminated soil. On the other hand, inoculation with LCC04, LCC69, LCC81 and IPA403 contributed to decrease qCO2.

Figure 4
Soil respiration (a) MBC (b) and respiratory quotient (c) after inoculation of maize with PGPB in soil with (+Cr) and without (–Cr) Cr.

The results showed, in general, a positive influence from inoculation on soil respiration and MBC. There are few reports about the effect of PGPR on soil microbial biomass and respiration, but these results agree with Sharma et al. (2013)Sharma, S. B., Sayyed, R. Z., Trivedi, M. H., and Gobi, T. A. (2013). Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. Springer plus, 2, 587. https://doi.org/10.1186/2193-1801-2-587
https://doi.org/10.1186/2193-1801-2-587...
, who reported that inoculation with Bradyrhizobium amyloliquefaciens significantly increased these parameters compared to uninoculated controls. Thus, the results add more information about the effect of PGPR on soil microbial biomass and activity, mainly under Cr-contamination. Interestingly, inoculation with LCC69 contributed to higher soil respiration and MBC in Cr-contaminated soil. Since soil respiration is recognized as a useful indicator of microbial activity (Alef and Nanipieri 1995Alef, K., and Nannipieri, P. (1995). Methods in Applied Soil Microbiology and Biochemistry. New York: Academic Press. https://doi.org/10.1016/B978-012513840-6/50014-8
https://doi.org/10.1016/B978-012513840-6...
), these results suggest that LCC69 could stimulate soil microbial biomass and activity in Cr-contaminated soil. In Cr-contaminated soil, microbial biomass decreased, while qCO2 increased in uninoculated soil. This suggests that high Cr contamination inhibits microbial biomass and causes soil microbial stress (Sousa et al. 2017Sousa, R. S., Santos, V. M., Melo, W. J., Nunes, L. A. P. L., Van den Brink, P. J., and Araújo, A. S. F. (2017). Time-dependent effect of composted tannery sludge on the chemical and microbial properties of soil. Ecotoxicology, 26, 1366-1377. https://doi.org/10.1007/s10646-017-1861-9
https://doi.org/10.1007/s10646-017-1861-...
).

Finally, the results of this study showed a differential response of several potential PGPR on maize growth and accumulation of Cr, and microbial biomass under noncontaminated and Cr-contaminated soils, in a pot-experiment. This study highlights the potential of these isolates to promote plant growth even in contaminated soils. Since this study was conducted in a controlled greenhouse experiment, further studies under field conditions, different soil types and plant species are necessary to potentially recommend these isolates as inoculants to be used by farmers. However, research under controlled conditions is one of the first steps required to identify potential strains prior to evaluation under field conditions. For example, Antunes et al. (2011)Antunes, J. E. L., Gomes, R. L. F., Lopes, A. C. A., Araújo, A. S. F., Lyra, M. C. C. P., and Figueiredo, M. V. B. (2011). Eficiência simbiótica de isolados de rizóbio noduladores de feijão-fava (Phaseolus lunatus L.). Revista Brasileira de Ciência do Solo, 35, 751-757. https://doi.org/10.1590/S0100-06832011000300011
https://doi.org/10.1590/S0100-0683201100...
evaluated the responses of rhizobia on growth of lima bean, under a greenhouse, and identified potential isolates to be used under field conditions. Later, Costa et al. (2020)Costa, C. N., Antunes, J. E. L., Lopes, A. C. A., Freitas, A. D. S., and Araujo, A. S. F. (2020). Inoculation of rhizobia increases lima bean (Phaseolus lunatus) yield in soils from Piauí and Ceará states, Brazil. Revista Ceres, 67, 419-423. https://doi.org/10.1590/0034-737x202067050010
https://doi.org/10.1590/0034-737x2020670...
assessed these isolates on lima bean yield, under field conditions and two locations, and found two strains to be recommended as effective inoculants for this crop.

CONCLUSION

Plant growth-promoting rhizobacteria isolated from Cr-contaminated soils present the potential to promote plant growth, reduce translocation of Cr within the plant and improve soil microbial biomass and activity. Particularly, LCC41 and LCC81 could potentially promote maize growth and reduce Cr accumulation in shoots, respectively, in Cr-contaminated soil. In addition, LCC69 stimulated microbial biomass and activity. Further studies should be done aiming to verify the performance of these PGPR on Cr degradation.

ACKNOWLEDGMENTS

The authors thank CAPES for the scholarship to Raquel Sobral Silva and Jadson Emanuel Lopes Antunes. Ademir Sergio Ferreira de Araujo and Wanderley José de Melo thank CNPq for their research fellowship.

  • How to cite: Silva, R. S., Antunes, J. E. L., Aquino, J. P. A., Sousa, R. S., Melo, W. J. and Araujo, A. S. F. (2021). Plant growth-promoting rhizobacteria effect on maize growth and microbial biomass in a chromium-contaminated soil. Bragantia, 80, e2521. https://doi.org/10.1590/1678-4499.20200492
  • DATA AVAILABILITY STATEMENT

    Data will be available upon request.
  • FUNDING

    Conselho Nacional de Desenvolvimento Científico e Tecnológico
    Grant No. 305069/2018-1
    Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
    Finance Code 001

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Edited by

Section Editor: Hector Valenzuela

Publication Dates

  • Publication in this collection
    03 May 2021
  • Date of issue
    2021

History

  • Received
    01 Dec 2020
  • Accepted
    10 Mar 2021
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