Ecology

Sampling of organisms and bioassay experiments
Shrimp post-larvae (PL5) of Litopenaeus vannamei were collected from the aquaculture farm Parque acuícola Cruz de Piedra, Guaymas, Sonora, Mexico (27° 51′ 05.9″ N 110° 31′ 57.0″ W). Afterward, post-larval shrimp were transported in aerated tanks with the same pond water as the farm to the Departamento de Investigaciones Científicas y Tecnológicas de la Universidad de Sonora (DICTUS), where a lab-scale system was previously tested and used. The bioassay was conducted for 80 days with healthy shrimp, each weighing 0.5 ± 0.1 g, and post-larvae were randomly distributed in the lab-scale system. The system consisted of nine 80-L culture units linked to a recirculation aquaculture system (RAS), and sterile seawater was used to fill the units to an operating volume of 60 L. Influent seawater was filtrated and flowed through a UV lamp for sterilization, and the seawater was equally dispensed to all culture units, as depicted in the supplementary material (Fig. S2). The culture units were maintained under similar indoor conditions with artificial aeration (2000F heat bonded silica; pore size, 140 µm), and the salinity was maintained at around 35‰ with the addition of sterile freshwater (MilliQ grade, Millipore) to avoid the incorporation of outside bacteria and to compensate evaporation. Finally, the effluent generated by the system flowed through a biofilter containing nitrifying bacteria to control toxic nitrogen compounds in the recirculation system (Fig. S2). The unconsumed feed, feces, moults, and dead organisms (if any) were removed daily.
The salinity, dissolved oxygen (DO), pH, and temperature were measured twice per day (07:00 and 18:00 h) using a YSI multiprobe system 556 (YSI Incorporated).
The bioassay started with PL5 on day 0. At this point, 40 organisms were randomly introduced into each culture unit, and the experiment lasted 80 days. Throughout the experiment, shrimp were fed twice a day at a rate of 4% wet biomass day–1 using feeding trays with the same formulated feed consisting of commercial grow-out pelletized feed with 25% crude protein, 5% lipids, and 4% fiber.
Water quality and productive response
The water quality was monitored daily throughout the bioassay, and samples were collected weekly from each culture unit using sterile falcon tubes by filtering the water through 0.45 μm membranes (Millipore). Nitrite (NO2–N), nitrate (NO3–N), ammonia (NH3–NH4), and phosphate (P–PO4) concentrations were measured using commercial Hanna reagent kits HI 93707-01, HI 93728-01, HI 93700-01, and HI 93717-01, respectively (Hanna Instruments, Romania).
Biometry analyses were performed at the four different developmental stages, denominated as I, II, III, and IV, corresponding to 0–20, 20–40, 40–60, and 60–80 culture days, respectively, and the productive response was calculated15.
Collection of intestine and water samples and DNA and RNA extraction
To discard the transitory microbiota, the shrimp were fasted for 6 h before sampling. Once the intestines were empty, these were dissected on the corresponding dates using a sterile dissection kit, placed in sterile cryogenic tubes, and stored at – 80 °C until nucleic acid extraction. Each sample date belongs to an experimental unit with three culture tanks. The intestine samples from culture tanks were pooled and considered as a replicate, giving three replicates per sampling time. At the same sampling points, 1 L samples of water (W) from each culture unit corresponding to an experimental replicate were collected and pooled for filtration through 0.22 µm sterile filters of mixed cellulose ester membrane (Whatman, Sigma, St Louis, USA) and placed in sterile, 50 mL falcon tubes for storage at – 80 °C until nucleic acid extraction.
Total DNA and RNA were extracted and purified from the membrane filters previously used to filter seawater samples and from intestines that were also previously sampled, both of them with the FastDNA Spin Kit for Soil15, and the FastRNA Pro Blue Kit (MP-Bio, Santa Ana, CA, USA) in combination with mechanical lysis using the FastPrep Systems (MP-BIO, Santa Ana, CA, USA). The obtained RNA samples were digested according to the TURBO DNA protocol (Ambion, Life Technologies Corporation, Carlsbad, CA, USA) and EDTA to stop the DNase activity and to ensure that any DNA residuals were presented. Finally, samples were purified according to the RNA Cleanup protocol from the RNeasy Mini Kit (Qiagen, Hamburg, Germany). The quality and concentration of nucleic acids were tested as previously described Maza-Márquez et al.39.
qPCR and RT-qPCR assays
Real-time polymerase chain reaction (qPCR) assays have been widely implemented for estimating total cell count based on DNA gene markers, regardless of their level of metabolic activity40,41, while reverse transcription qPCR (RT-qPCR) is a useful method for analyzing the expression of specific genes. RT-qPCR is also used because of its high sensitivity, accuracy, specificity, and rapidity in analyzing the time-specific expression of particular genes, allowing for the detection of low-abundance transcripts42. The absolute abundance of total and metabolically active populations of bacteria and Vibrio in both target samples were measured by qPCR and RT-qPCR, respectively, using a StepOne Real-Time PCR system (Applied Biosystems, USA). For RT-qPCR, the synthesis of cDNA was performed by reverse transcription of RNA with the aid of SuperScript III Reverse Transcriptase (Invitrogen, Life Technologies Corporation, Carlsbad, CA, EEUU), following the manufacturer’s specifications, in a final volume of 20 µL and using 150–200 ng of total RNA as a template (specific primers described in Table S4) (Sigma Aldrich; St. Louis, MO, USA) and dNTPs (Invitrogen; Carlsbad, USA). In addition, the cDNA quality and concentration were measured using a NanoDrop ND-1000 spectrophotometer (Thermo Scientific Waltham, MA USA). The number of copies (nbc) of 16S rRNA genes (16S rDNA) and 16S rRNA (16S rRNA) were evaluated in each sample using either extracted DNA or cDNA, respectively, as templates with a set of primers previously described (Table S4) based on the increasing fluorescence intensity of the SYBR Green dye during amplification. For the amplification and detection of specific fragments, the iTaq Universal SYBR Green Supermix (Biorad, USA) was used in a final volume of 15 µL for each reaction. All quantitative amplifications were performed in triplicate. The qPCR reaction mixtures contained 1.8 µL of cDNA or DNA, 250 ng of T4 gene 32 (QBiogene, Illkirch, France), 1.2 µL of each primer (10 mM), supplied by Sigma Aldrich (St. Louis, MO, USA), and 1 × SYBR Green Supermix. The amplification and detection conditions are described in Table S5.
To provide absolute quantification of the target microorganisms, standard curves were constructed with the aid of a standard plasmid that contained the inserts of the targeted genes. Amplicons of the 16S rDNA were generated from culture strains of Pseudomonas putida NCB957 (quantification of bacteria) and Vibrio parahaemolyticus ATCC17802 (quantification of Vibrio). The PCR products were cloned with the aid of the pCR2.1-TOPO plasmid vector using the TOPO TA cloning system (Invitrogen, Life Technologies Corporation, Carlsbad, CA, USA), following the manufacturer’s protocols. The calibration curves for absolute quantification in the DNA samples (16S rDNA) were generated using serial ten-fold dilutions of linearized plasmid standards, and for absolute quantification in RNA samples (16S rRNA), non-linearized plasmid standards were used as templates for in vitro transcription of the target genes into RNA39,40,43. The copy number per ng was calculated as previously described43. All calibration curves had a correlation coefficient (r2) of  > 0.99 in all assays, and the efficiency of PCR amplification was always between 90 and 110%. Finally, the number of copies of the targeted genes was expressed per gram of tissue sampled, while for water samples these were expressed as the number of copies per mL.
Statistical analyses
All statistical analyses were performed in R Studio (version 3.6.0)44 using the following R packages: maggrittr45, ade446, factoextra47, vegan48, and gplots49. Analyses of variance (ANOVA) and multiple-range tests (Student’s-test) were used with a significance level of 95% (p  More

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Surface water frequency maps and surface water areas during 1989–2016
Surface water frequencies (FW) of individual pixels in 2016 varied substantially across China (Fig. 1a). There were 1444 million pixels with annual surface water frequency of FW  > 0 in 2016, amounting to ~1.3 × 106 km2 maximum SWA in 2016. Based on the surface water frequency in a year, a water pixel was defined as year-long surface water (FW ≥ 0.75), seasonal surface water (0.05 ≤ FW  More

Study site
This study was conducted in Shenmu County of Shaanxi Province in China (110° 05′–110° 30′ E, 39° 27′–39° 15′ N), which is located in the continental arid and Semiarid areas. The annual average temperature is 8.9 °C. The annual frost-free period is 130 days, the mean annual precipitation of the area is about 396 mm, and potential evaporation is 1,790 mm.
The research plot is in the heartland of Shendong coal mining subsidence area in Shenmu County, typical steppe landscape, soil impoverishment, and fragile ecological environment. The basic physical soil properties in the test site were measured (Table 1). According to the SL237-1999 engineering classification standard of the Geotechnical Test Regulations, the soil in the test area was named as low liquid limit silt (ML). Major plant species under natural conditions in the study area include S. psammophila, Caragana microphylla Lam., H. rhamnoides L., Artemisia ordosica Krasch., Agriophyllum squarrosum (Linn. ) Moq., and Lespedeza bicolor Turcz.
Table 1 Basic physical properties of soil in the test area.
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Root sampling
The straight roots of 4 years old of S. psammophila and H. rhamnoides L. were used as materials, and applied instantaneous axial small injured force (corresponding to 30% of the average ultimate force of the radial level, less than the elastic ultimate force, and the deformation is recoverable elastic deformation) and instantaneous axial large injured force (corresponding to 70% of the average ultimate force of the radial level, greater than the elastic ultimate force, and the deformation is irreversible plastic deformation) without leaving the plant body, to understand the survival rate, the change in root diameter and tensile strength of straight roots withstand transient tensile injured after self-repair.
As the layers of soil could interfere with the anti-tension force and anti-tension strength of roots, we excavated the roots without leaving the plant body and selected the roots which are distributed in the same soil layer. Straight roots with uniform diameter ranged from 1 to 4.5 mm, roots segments of 100 mm were selected from the root systems. To sufficiently attribute the tensile ability of roots, the selected roots were divided into seven diameter classes with 0.5 mm interval. To ensure the parallelism of the test, each diameter class selected eight test roots and eight control roots.
In the test, the soil around test roots was removed and the position of test roots was kept unchanged so that the exposed length of the roots reached the test requirements, the test roots were shaded, and sprayed water to maintain moisture. And each test root length was greater than 100 mm (Fig. 1), three points of A, B and C was selected along the root, and the diameters were measured by the cross method using an electronic Vernier caliper with an accuracy of 0.01 mm. B was the midpoint of the test root, A, C were the ends of the 30 mm from the midpoint. The diameters of control roots were measured in the same way.
Figure 1

The schematic diagram of test root.

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Root treatments
At the beginning of the plant growing season, in 2019 May. Test roots were applied two instantaneous axial injured forces without leaving the plant body, then covered soil growth. The process of excavation and covering soil was also carried out on the control roots in the same way (Fig. 1). By August, after a 3-month growth period, the test roots self-repaired for 3 months and excavated the test roots and control roots again, observed the survival rate, measured the root diameter and the tensile strength of test root (Fig. 2).
Figure 2

Excavation phase of test roots.

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Root tensile tests were conducted by a homemade portable instrument (Fig. 3). The instrument is composed with a platform (Part A), a root clap (Part B) fixed on the platform, a HG 100 digital display type push–pull meter (Part C), a moveable root clap (Part D) which is connected with Part C, a crank handle (Part E) which is used to move Part C and a Vernier caliper (Part F) which is connected with Part C to control the loading rate of the load. The test root is clapped by the two root pads. To make sure the test root not slip, we put a rubber pad inside each of the root clap. When the crank handle is turned, Part C is moved away from Part B and the force acted on the test root is recorded. The accuracy of HG 100 digital display type push–pull meter is 0.05 N. After selecting the test root, carefully excavated the soil under the test root and placed the instrument (length 50 cm, width 13 cm, height 20 cm). Fixed the points a and c of the test root at the jaws of the clamp so that the test root was in tension. The axial direction was pulled, and the length of the instrument was placed in the same direction as the root growth direction. Using 50 mm/min loading rate applied force injury by reading the Vernier caliper moving rate, stopped after the degree of injury urging force of the design, marked the ends of the test root segment and backfilled them, and marked on the ground to be dug again. The treatment method of the parallel control test roots was the same.
Figure 3

HG 100 digital display type push–pull meter and self-made portable test instrument.

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Determination of injury force
The recoverable elastic deformation occurs in the root system before the elastic limit point. After the elastic limit point, the root system undergoes irreversible plastic deformation. Previous researches indicate that the elastic limit of the 0–8 mm straight root of S. psammophila is about 40% of the ultimate tensile strength, and that of H. rhamnoides L. is about 60% of the ultimate tensile strength30,31. Tests have shown that when the injury force reaches 80% of the average ultimate tensile strength, more test roots break when applying the injury forces. To observe impact of varied injury force on the self-repair of roots, we selected two levels of injury force in this study, the small injury force was 30% of the ultimate tensile force (less than the elastic limit point), and the large injury force was 70% of the ultimate tensile force (greater than the elastic limit point).
Due to the uneven root diameter along the axial direction, it was impossible to determine the fracture point at which the test root may be damaged before the test. To guarantee data quality, the measured number was not recorded when the test root was fractured in the experiment. The ultimate force was calculated from the regression equation according to the average root diameter of each test root test segment, the average root diameter of each test root was the mean of the root diameters of the three points A, B, and C. According to the root diameter of each test root, the ultimate tensile force was calculated by the regression equation, and the corresponding small injury force and large injury force were determined (Table 2).
Table 2 Ultimate anti-fracture force and its regression equation with root diameter of two plants.
Full size table

Data analysis
The data were analyzed using SPSS 15.0 for Windows. The test roots and the parallel control roots were excavated after self-repaired for 3 months, observed the root shape, color and elasticity. If the root turned black, dry and begins to fall off, the root was dead. For the roots that survived, the root diameter and ultimate tensile strength were measured again, and the tensile strength was calculated using Eq. 1.

$$ {text{P}} = 4{text{F}}/left( {uppi {text{D}}^{2} } right) $$
(1)

where P is the tensile strength (MPa), F is the tensile force (N), D is the root diameter (mm). More

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