Effect of insect-resistant transgenic rice and its hybrid combination rice on diversity and composition of soil microbial community
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摘要: 微生物是土壤物质循环与肥力演变的驱动者, 其群落组成关系到土壤微生态系统的稳定与可持续性。对抗虫转基因水稻土壤微生物群落变化的研究是其环境安全性评价的重要内容。本研究基于细菌16S rRNA基因和真菌ITS基因的高通量测序, 分析了田间试验中抗虫转基因水稻‘MFB’及其转基因杂交水稻‘闽丰A/MFB’ ‘天丰A/MFB’和‘谷丰A/MFB’与非转基因常规水稻‘闽恢3301’及杂交水稻‘天优华占’的土壤微生物群落多样性与组成的差异, 并得出以下结果。首先, 与非转基因常规水稻‘闽恢3301’或杂交水稻‘天优华占’相比, 抗虫转基因水稻‘MFB’及转基因杂交水稻‘闽丰A/MFB’ ‘天丰A/MFB’和‘谷丰A/MFB’均能显著增产(P<0.05)。同时, 高通量测序结果表明, 除水稻成熟期的土壤真菌群落外, 与‘闽恢3301’相比 ‘MFB’的土壤细菌或真菌群落的α-多样性指数Chao1、Observed_species和Shannon均有所提高, 且分别在水稻成熟期或分蘖期达到显著性水平(P<0.05); 水稻齐穗期时转基因杂交水稻‘闽丰A/MFB’ ‘天丰A/MFB’和‘谷丰A/MFB’的土壤细菌及真菌群落的多样性指数Shannon均介于‘MFB’与‘天优华占’之间; 微生物群落β-多样性分析结果表明, 本田间试验中不同品种水稻土壤细菌或真菌的群落组成均没有显著差异。但与‘闽恢3301’相比, 稻田土壤细菌中丰度最高的变形菌门(Proteobacteria)的相对丰度在‘MFB’土壤中明显增加, 且在水稻分蘖期及成熟期时达到显著性水平(P<0.05), 而土壤真菌中丰度最高的子囊菌门(Ascomycota)的相对丰度在‘MFB’土壤中明显减少, 且在水稻分蘖期及齐穗期时差异显著(P<0.05); 水稻齐穗期时, ‘闽丰A/MFB’ ‘天丰A/MFB’和‘谷丰A/MFB’的土壤变形菌门或子囊菌门的相对丰度也均介于‘MFB’与‘天优华占’之间。此外, 通过对微生物群落的功能组成预测可见, 随水稻生长, ‘MFB’与‘闽恢3301’的土壤细菌群落功能组成间差异存在增大的趋势。综上所述, 本研究田间试验中, 抗虫转基因水稻及其转基因杂交水稻在增产的同时提高了稻田土壤细菌或真菌群落的多样性, 改变了主要细菌或真菌种类的相对丰度, 但对细菌或真菌的群落及功能组成的影响不显著。Abstract: Microorganisms are the drivers of soil material cycle and fertility evolution, and their community composition is related to the stability and sustainability of soil microecosystems. The study of soil microbial community changes in insect-resistant transgenic rice is an important part of its environmental safety assessment. Based on high-throughput sequencing of bacterial 16S rRNA gene and fungal ITS gene, this study analyzed the differences in diversity and composition of microbial communities in paddy soils of field experiment between with insect-resistant transgenic rice ‘MFB’, insect-resistant transgenic hybrid rice ‘Minfeng A/MFB’ ‘Tianfeng A/MFB’ or ‘Gufeng A/MFB’ and with non-transgenic conventional rice ‘Minhui 3301’ or hybrid rice ‘Tianyouhuazhan’. The results showed, firstly, compared with non-transgenic conventional rice ‘Minhui 3301’ or hybrid rice ‘Tianyouhuazhan’, both insect-resistant transgenic rice ‘MFB’ and transgenic hybrid rice ‘Minfeng A/MFB’ ‘Tianfeng A/MFB’ or ‘Gufeng A/MFB’ could significantly increase rice yield (P<0.05). At the same time, except for the soil fungal communities during the rice maturation stage, the result of high-throughput sequencing showed that the α-diversity index of Chao1, Observed_species and Shannon of bacterial or fungal communities in paddy soil with ‘MFB’ were all higher than those of with ‘Minhui 3301’, and the most significant in rice maturation stage or tillering stage respectively (P<0.05). At the heading stage of rice, the Shannon index of bacterial or fungal communities in paddy soils with the insect-resistant transgenic hybrid rice ‘Minfeng A/MFB’ ‘Tianfeng A/MFB’ or ‘Gufeng A/MFB’ were between those of with ‘MFB’ and ‘Tianyouhuazhan’. The results of β-diversity analysis of bacterial or fungal communities showed there were no significant differences in the composition of microbial communities in paddy soils with different varieties of rice in this field experiment. However, compared with ‘Minhui 3301’, the relative abundance of Proteobacteria with the highest abundance of bacteria increased in the paddy soil with ‘MFB’, and reached the significance level at the tillering and maturation stages of rice (P<0.05), while the relative abundance of Ascomycota with the highest abundance of fungi decreased in the paddy soil with ‘MFB’, and reached the significance level at the tillering and heading stages of rice (P<0.05). At the heading stage of rice, the relative abundance of Proteobacteria or Ascomycota in paddy soils with ‘Minfeng A/MFB’ ‘Tianfeng A/MFB’ or ‘Gufeng A/MFB’ were between those of with ‘MFB’ and ‘Tianyouhuazhan’. According to the functional prediction of microbial communities, the differences in functional composition of bacterial communities in paddy soil between with ‘MFB’ and ‘Minhui 3301’ gradually increased along with the rice growth. In summary, in the field experiment of this study, insect-resistant transgenic rice and its transgenic hybrid rice increased the diversity of soil bacterial or fungal communities, changed the relative abundance of major species of bacteria or fungi with increasing rice yield, but did not have significant effects on the community and functional composition of bacteria or fungi.
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图 1 水稻不同生育期稻田土壤细菌群落β-多样性的主坐标分析
A: ‘闽丰A/MFB’; B: ‘天丰A/MFB’; C: ‘谷丰A/MFB’; D: ‘天优华占’; E: ‘MFB’; F: ‘闽恢3301’。A: ‘Minfeng A/MFB’; B: ‘Tianfeng A/MFB’; C: ‘Gufeng A/MFB’; D: ‘Tianyouhuazhan’; E: ‘MFB’; F: ‘Minhui 3301’.
Figure 1. Principal co-ordinates analysis for beta diversity of bacterial communities in paddy soil at different growth stages of rice
图 2 水稻不同生育期稻田土壤真菌群落β-多样性的主坐标分析
A: ‘闽丰A/MFB’; B: ‘天丰A/MFB’; C: ‘谷丰A/MFB’; D: ‘天优华占’; E: ‘MFB’; F: ‘闽恢3301’。A: ‘Minfeng A/MFB’; B: ‘Tianfeng A/MFB’; C: ‘Gufeng A/MFB’; D: ‘Tianyouhuazhan’; E: ‘MFB’; F: ‘Minhui 3301’.
Figure 2. Principal co-ordinates analysis for beta diversity of fungal communities in paddy soil at different growth stages of rice
图 3 水稻不同生育期稻田土壤主要细菌门的相对丰度
不同小写字母表示相同菌门不同处理在P<0.05 水平差异显著。Different lowercase letters mean significant differences among different treatments of the same bacterial phylum at P<0.05 level .
Figure 3. Relative abundance of main bacterial phylum in paddy soil at different growth stages of rice
图 4 水稻不同生育期稻田土壤主要真菌门的相对丰度
不同小写字母表示相同菌门不同处理在P<0.05 水平差异显著。
Figure 4. Relative abundance of main fungal phylum in paddy soil at different growth stages of rice
Different lowercase letters mean significant differences among different treatments of the same fungal phylum at P<0.05 level.
图 5 水稻不同生育期稻田土壤细菌群落的物种组成聚类热图
A: ‘闽丰A/MFB’; B: ‘天丰A/MFB’; C: ‘谷丰A/MFB’; D: ‘天优华占’; E: ‘MFB’; F: ‘闽恢3301’。A: ‘Minfeng A/MFB’; B: ‘Tianfeng A/MFB’; C: ‘Gufeng A/MFB’; D: ‘Tianyouhuazhan’; E: ‘MFB’; F: ‘Minhui 3301’.
Figure 5. Cluster heat map of bacterial communities in paddy soil at different growth stages of rice
图 6 水稻不同生育期稻田土壤真菌群落的物种组成聚类热图
A: ‘闽丰A/MFB’; B: ‘天丰A/MFB’; C: ‘谷丰A/MFB’; D: ‘天优华占’; E: ‘MFB’; F: ‘闽恢3301’。A: ‘Minfeng A/MFB’; B: ‘Tianfeng A/MFB’; C: ‘Gufeng A/MFB’; D: ‘Tianyouhuazhan’; E: ‘MFB’; F: ‘Minhui 3301’.
Figure 6. Cluster heat map of fungal communities in paddy soil at different growth stages of rice
图 7 水稻不同生育期稻田土壤细菌群落功能单元主坐标分析
A: ‘闽丰A/MFB’; B: ‘天丰A/MFB’; C: ‘谷丰A/MFB’; D: ‘天优华占’; E: ‘MFB’; F: ‘闽恢3301’。A: ‘Minfeng A/MFB’; B: ‘Tianfeng A/MFB’; C: ‘Gufeng A/MFB’; D: ‘Tianyouhuazhan’; E: ‘MFB’; F: ‘Minhui 3301’.
Figure 7. Principal co-ordinates analysis for functional unit of bacterial communities in paddy soil under different growth stages of rice
图 8 水稻不同生育期稻田土壤真菌群落功能单元主坐标分析
A: ‘闽丰A/MFB’; B: ‘天丰A/MFB’; C: ‘谷丰A/MFB’; D: ‘天优华占’; E: ‘MFB’; F: ‘闽恢3301’。A: ‘Minfeng A/MFB’; B: ‘Tianfeng A/MFB’; C: ‘Gufeng A/MFB’; D: ‘Tianyouhuazhan’; E: ‘MFB’; F: ‘Minhui 3301’.
Figure 8. Principal co-ordinates analysis for functional unit of fungal communities in paddy soil under different growth stages of rice
表 1 不同品种水稻的产量性状
Table 1. Yield characteristics of different rice varieties
水稻品种
Rice variety有效穗数
Effective panicle number结实率
Setting rate (%)千粒重
1000-grain weight (g)单株产量
Yield per plant (g∙plant−1)‘闽丰A/MFB’ ‘Minfeng A/MFB’ 11.8±1.2ab 71.7±5.4a 30.7±0.5a 57.9±6.2a ‘天丰A/MFB’ ‘Tianfeng A/MFB’ 12.2±1.0a 64.6±1.9b 31.8±0.7a 55.7±5.1a ‘谷丰A/MFB’ ‘Gufeng A/MFB’ 9.9±1.2b 62.4±5.2bc 33.7±1.6a 44.8±6.1b ‘天优华占’ ‘Tianyouhuazhan’ 11.4±2.2ab 45.9±3.6d 33.4±3.9a 32.7±10.1cd ‘MFB’ 11.9±1.1a 58.1±3.0c 30.6±1.9a 41.4±8.2bc ‘闽恢3301’ ‘Minhui 3301’ 12.8±2.0a 51.6±3.2d 30.9±4.8a 27.6±6.6d 同列不同小写字母表示同一指标在不同品种间差异显著(P<0.05)。Lowercase letters in the same column refer to significant difference of the same indicator for different rice varieties (P<0.05). 
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表 2 水稻不同生育期稻田土壤细菌群落的α-多样性指数
Table 2. Alpha diversity index of bacterial communities in paddy soil under different growth stages of rice
生育期
Growth stage水稻品种
Rice variety丰富度指数 Richness index 多样性指数 Diversity index 均匀度指数
Pielou_eChao1 Observed_species 香农多样性指数
Shannon辛普森多样性指数
Simpson分蘖期
Tillering stage‘闽丰A/MFB’
‘Minfeng A/MFB’5842±815a 5310±495ab 11.20±0.13ab 0.9987±0.0001c 0.9054±0.0022b ‘天丰A/MFB’
‘Tianfeng A/MFB’5552±201a 4929±99b 11.10±0.01b 0.9990±0.0000b 0.9047±0.0011b ‘谷丰A/MFB’
‘Gufeng A/MFB’5718±288a 5116±140ab 11.21±0.03ab 0.9991±0.0000a 0.9097±0.0015a ‘天优华占’
‘Tianyouhuazhan’5753±326a 4970±186b 11.19±0.05ab 0.9991±0.0000a 0.9112±0.0002a ‘MFB’ 6286±214a 5501±134a 11.30±0.03a 0.9991±0.0000a 0.9096±0.0010a ‘闽恢3301’
‘Minhui3301’5731±502a 4937±342b 11.10±0.11b 0.9990±0.0001b 0.9047±0.0020b 齐穗期
Heading stage‘闽丰A/MFB’
‘Minfeng A/MFB’6481±133a 6131±116ab 11.04±0.03a 0.9982±0.0001a 0.8777±0.0029b ‘天丰A/MFB’
‘Tianfeng A/MFB’6280±211a 5796±178ab 10.76±0.01b 0.9960±0.0001c 0.8611±0.0024c ‘谷丰A/MFB’
‘Gufeng A/MFB’6450±240a 6124±180ab 10.76±0.04b 0.9961±0.0002c 0.8550±0.0018d ‘天优华占’
‘Tianyouhuazhan’5971±169a 5692±197b 10.68±0.12b 0.9959±0.0006c 0.8563±0.0060cd ‘MFB’ 6492±295a 6221±215a 11.06±0.04a 0.9972±0.0001b 0.8773±0.0022b ‘闽恢3301’
‘Minhui3301’6012±621a 5684±491b 11.03±0.07a 0.9981±0.0001a 0.8847±0.0034a 成熟期
Maturation stage‘闽丰A/MFB’
‘Minfeng A/MFB’5051±357c 4879±295c 10.87±0.09c 0.9980±0.0002b 0.8876±0.0019b ‘天丰A/MFB’
‘Tianfeng A/MFB’5120±20c 4980±40c 11.00±0.04b 0.9985±0.0001a 0.8960±0.0025a ‘谷丰A/MFB’
‘Gufeng A/MFB’4730±130c 4551±119c 10.80±0.05c 0.9980±0.0001b 0.8888±0.0013b ‘天优华占’
‘Tianyouhuazhan’5157±478c 4897±352c 10.99±0.08b 0.9984±0.0001a 0.8969±0.0011a ‘MFB’ 6646±720a 6240±459a 11.23±0.07a 0.9983±0.0000a 0.8910±0.0020b ‘闽恢3301’
‘Minhui3301’5923±97b 5620±52b 11.05±0.04b 0.9981±0.0001b 0.8875±0.0029b 同列不同小写字母表示同一指标在不同品种间差异显著(P<0.05)。Different lowercase letters in the same column mean significant difference of the same indicator for different rice varieties (P<0.05).
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表 3 水稻不同生育期稻田土壤真群落的α-多样性指数
Table 3. Alpha diversity index of fungal communities in paddy soil under different growth stages of rice
生育期
Growth stage水稻品种
Rice variety丰富度指数
Chao1丰富度指数
Observed_species香农多样性指数
Shannon辛普森多样性指数
Simpson均匀度指数
Pielou_e分蘖期
Tillering stage‘闽丰A/MFB’
‘Minfeng A/MFB’254±2a 254±3a 5.94±0.12b 0.9605±0.0043b 0.7437±0.0136c ‘天丰A/MFB’
‘Tianfeng A/MFB’178±6c 178±5c 6.03±0.06ab 0.9725±0.0035ab 0.8070±0.0073a ‘谷丰A/MFB’
‘Gufeng A/MFB’245±28a 245±28a 6.26±0.30ab 0.9740±0.0082a 0.7894±0.0215ab ‘天优华占’
‘Tianyouhuazhan’223±3b 222±3b 6.33±0.12a 0.9751±0.0032a 0.8116±0.0172a ‘MFB’ 194±7c 193±7c 6.21±0.22ab 0.9776±0.0047a 0.8173±0.0241a ‘闽恢3301’
‘Minhui 3301’155±7d 154±6d 5.50±0.30c 0.9527±0.0136b 0.7569±0.0365bc 齐穗期
Heading stage‘闽丰A/MFB’
‘Minfeng A/MFB’654±48c 653±47c 6.19±0.48bc 0.9544±0.0271b 0.6618±0.0448bc ‘天丰A/MFB’
‘Tianfeng A/MFB’787±20b 783±22b 6.34±0.12b 0.9484±0.0037bc 0.6599±0.0097c ‘谷丰A/MFB’
‘Gufeng A/MFB’784±48b 775±45b 6.35±0.07b 0.9553±0.0024b 0.6617±0.0097bc ‘天优华占’
‘Tianyouhuazhan’696±44c 690±41c 5.91±0.10c 0.9341±0.0012c 0.6267±0.0052c ‘MFB’ 919±56a 906±56a 7.18±0.26a 0.9832±0.0038a 0.7310±0.0212a ‘闽恢3301’
‘Minhui 3301’852±13ab 840±16ab 6.79±0.13a 0.9758±0.0037a 0.6992±0.0124ab 成熟期
Maturation stage‘闽丰A/MFB’
‘Minfeng A/MFB’948±44ab 936±43ab 7.24±0.0ab 0.9825±0.0008a 0.7335±0.0046a ‘天丰A/MFB’
‘Tianfeng A/MFB’797±20c 796±18c 7.11±0.06b 0.9811±0.0009a 0.7376±0.0074a ‘谷丰A/MFB’
‘Gufeng A/MFB’972±70ab 954±65ab 7.24±0.15ab 0.9807±0.0048a 0.7316±0.0225a ‘天优华占’
‘Tianyouhuazhan’1038±54a 1013±54a 7.29±0.08a 0.9796±0.0038a 0.7304±0.0131a ‘MFB’ 884±102b 872±91b 7.27±0.09ab 0.9837±0.0005a 0.7442±0.0056a ‘闽恢3301’
‘Minhui 3301’943±107ab 922±97ab 7.33±0.14a 0.9832±0.0011a 0.7443±0.0043a 同一生长时期中同列不同小写字母表示同一指标在同一生长时期不同品种间差异显著(P<0.05)。Different lowercase letters in the same column at the same growth stage mean significant difference of the same indicator at the same growth stage for different rice varieties (P<0.05).
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