key: cord-0757740-vjojsm1r authors: Anand, Uttpal; Bianco, Francesco; Suresh, S.; Tripathi, Vijay; Núñez-Delgado, Avelino; Race, Marco title: SARS-CoV-2 and other viruses in soil: an environmental outlook date: 2021-05-07 journal: Environ Res DOI: 10.1016/j.envres.2021.111297 sha: 4f2971d8d5d8147f7363cb73f8d7db6bc2460d75 doc_id: 757740 cord_uid: vjojsm1r In the present review, the authors shed light on the SARS-CoV-2 impact, persistence, and monitoring in the soil environment. With this purpose, several aspects have been deepened: i) viruses in soil ecosystems; ii) direct and indirect impact on the soil before and after the pandemic, and iii) methods for quantification of viruses and SARS-CoV-2 monitoring in soil. Viruses are present in soil (i.e. up to 417×10(7) viruses per g TS(–1) in wetlands) and can affect the behavior and ecology of other life forms (e.g. bacteria), which are remarkably important for maintaining environmental equilibrium. Also, SARS-CoV-2 can be found in soil (i.e. up to 550 copies·g(–1)). Considering that the SARS-CoV-2 is very recent, poor knowledge is available in the literature on persistence in the soil and reference has been made to coronaviruses and other families of viruses. For instance, the survival of enveloped viruses (e.g. SARS-CoV) can reach 90 days in soils with 10% of moisture content at ambient. In such a context, the possible spread of the SARS-CoV-2 in the soil was evaluated by analyzing the possible contamination routes. During the COVID-19 pandemic, different basic essential parameters (e.g. national economics, 92 public health) are assessed (Hsiang et al., 2020; Rundle et al., 2020; Siche, 2020) . However, among 93 all the environmental concerns of the current situation, soil health can be predominant for living 94 organisms. Indeed, soil plays an important role in the decomposition degree of organic compounds, 95 maintaining the biogeochemical cycle (Nannipieri et al., 2017) . Also, the soil is one of the greatest 96 reservoirs of microorganisms (Breitbart and Rohwer, 2005 ; Rohwer et al., 2009), which are 97 responsible for a series of environmental chemistry reactions (Douglas, 2006) . However, viruses 98 (e.g. bacteriophages) can affect the bacterial population, causing detrimental effects on soil quality 99 (Srinivasiah et al., 2013 ) (see section 2.2). 100 Viruses found in the soil environment can have an impact on economy and production likely due to 101 an infectious cycle that helps the gene transformation process (Breitbart and Rohwer, 2005 ; Jain, 102 In such context, and regarding microbiota, the complexity of the soil ecosystems is meaningful to 117 be understood, due to the fact that all the interactions between the host and virus or pathogens can 118 occur in the soil through contact with host cells (Emerson, 2019; Munson-Mcgee et al., 2018) , 119 which leads to virus replication and progeny release (Iwanami et al., 2020) . In addition, the 120 physical-chemical demand of soil ecosystems considerably affected the virus-host interactions in 121 the soil, allowing virus mutation due to the host resistance phenomena over the years (Sime-122 Ngando, 2014) . 123 Several extraction methods (e.g. dispersed soil, aqueous two-phase partitioning) evaluating the 124 bacterial number expressed as average per unit of inorganic mass are reported in studies on soil 125 microbiology to cope with soil microheterogeneity, returning results fluctuating with various orders 126 of magnitude (i.e. from 1×10 8 to 1×10 10 ) (Insam, 2001 ). In addition, recent analytical methods 127 focusing on the soil virome (i.e. the assembly of viruses) led to examine the virus role (e.g. 128 coronaviruses) in the soil microbial communities (Gundy et al., 2009; Srinivasiah et al., 2008) . 129 environmental compartments such as the soil, being resistant to hostile conditions and water 218 treatments (Kumar et al., 2020c). 219 For example, Adenovirus arrives in the soil environment after sewage sludge amendment (Horswell 220 et al., 2010) , and are subsequently sorbed by the soil particles through electrostatic interactions due 221 to its isoelectric point (Table 1) , as suggested by Wong et al. (2013) . Adenovirus showed a T 90 222 value comprised between almost 9 and 51 d at 4 °C (Table 1) depending on the biosolid considered 223 (i.e. dairy and swine manure, respectively) (Wei et al., 2009) . Also, in this case, an increase of 224 temperature can allow a reduction of T 90 to approximately 4 d ( Hence, a substantial screening should be conducted on the wastewater effluents and sewage sludge 259 before their application in soils to prevent the COVID-19 migration to other environmental 260 latitude, season and hour) (Herman et al., 2020) . Likewise, the presence of high concentrations of 295 contaminants in environmental matrices (e.g. soil) due to the improper discharge of polluted 296 wastewaters (Papirio et al., 2014) viruses (e.g. SARS-CoV-2) to other compartments can be enhanced by excessive soil tillage, which 302 was reported to decrease OM content in soil of approximately 40% . 303 3 Direct and indirect impact on the soil before and after pandemic 304 The advent of the COVID-19 in the world determined the closure of several secondary and tertiary 305 sector activities (e.g. non-essential factories, tourism) as well as the reduction of traffic mobility due 306 to the lockdown measures enforced by national policies, thus improving the air quality and reducing 307 the dispersion of pollutants in soil or sediments (Table 2) (Table 2) , which is also supported by the reduction of SARS-313 CoV-2 abundance to zero, evaluated both in the middle and low-risk periods in soils sampled after 314 the adopted stringent measures . 315 In addition, the production of medical wastes (i.e. infected and uninfected) significantly raised after Soil chemical processes are of crucial importance for long-term sustainability of soils and the 347 overall environment. With that in mind and knowing that it affects to both living organisms and all 348 other components in that environmental compartment, this section mainly focuses on methods for 349 virus elution during the extraction process, virus concentration techniques, detection, and 350 quantification ( Figure 3 and Table 3 ). 351 The first step to be followed for the quantification of viruses in soil matrices is the elution protocol 353 (Table 3) (Table 3) . 365 Other studies used four different elution buffers for phages in soil samples, specifically 1% 366 potassium citrate, 250 mM glycine buffer, 10% beef extract, and 10 mM sodium pyrophosphate, 367 and found 29% viable phages recovery using glycine and beef extract buffers ( (Table 3) . Similarly, 70% of recovery of rotavirus can be 393 obtained employing the PEG precipitation method at neutral pH, 15% concentration of PEG, and 394 protocol design for concentrating viral particles through UF and PEG techniques in soil samples 397 (Table 3) . Briefly, viral particles are taken after reinitializing and subsequently filtered through the 398 diafiltration system. Afterwards, this retentate is re-concentrated through UF and PEG precipitation. soil samples by precipitation with NaCl (0.3 mol·L -1 ) and PEG 6,000 (10%) overnight (Table 3) . 405 Humic acid (HA) negatively charged membrane is another method for concentrating viral particles 406 (Table 3) (2009) found 70 and 5% viral spherical particle, and tailed phages, respectively, in an agricultural 428 soil sample (Table 3 ). To be noted that, from TEM images, these researchers reported several non-429 tailed in addition to the tailed phages. 430 Hence, the HA membrane method represents a promising approach for obtaining metagenomic data 431 of virus particles from soil samples compared to UF and PEG. Thus, the HA membrane can be 432 considered the most suitable concentration method due to the low required background material in 433 the electron micrographs, and also for recovering various morphotypes and viruses. 434 In general, after elution and concentration of viral particles, virus detection methods (e.g. cell 436 culture, molecular techniques) are used for quantification of infectious viruses (Table 3) In the current COVID-19 pandemic, different basic essential parameters, mostly focusing on public 527 health, are generally assessed. However, soil health, which plays a major role in bacterial growth, 528 should be carefully evaluated to maintain environmental equilibrium. Indeed, these bacteria 529 populations can be affected by viruses that are transmitted from infected water bodies such as 530 untreated sewage, sewage sludge, and irrigation systems. This could deeply affect soil health likely 531 due to a variety of phenomena, including strong adsorption-desorption of viruses such as SARS-532 CoV-2. In such a context, the improper treatment of wastewater would pose a threat to human and 533 animal health. The viral load of enveloped viruses such as CoV could be maintained for a prolonged 534 time in the soil environment in the function of different parameters such as the temperature, 535 moisture content, pH, OM, sunlight radiation, and occurrence of clays and nutrients. Moreover, the 536 characteristics of enveloped viruses (e.g. SARS-CoV-2) can influence the virus's mobility in the soil 537 environment. Thus, the presence of SARS-CoV-2 could be directly monitored in soil matrices in-538 situ or with soil sampling for performing lab analyses after extraction and quantification methods 539 (e.g. elution protocol, PEG, PCR). Therefore, future studies about SARS-CoV-2 should be 540 especially aimed at focusing soil characteristics in order to cope with the COVID-19 pandemic and 541 long-term sustainability. 542 The authors declare that they have no known competing financial interests or personal relationships 545 that could have appeared to influence the work reported in this paper. 546 J o u r n a l P r e -p r o o f of the reported data for each soil. The virus to bacteria ratio (VBR) was calculated assuming a 1158 conversion factor of 1 g·mL -1 for bacterial abundance (Srinivasiah et al., 2008) . Data were taken 1159 from Williamson et al. (2017 Williamson et al. ( , 2007 Williamson et al. 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