Response of Bacterial Community in Soil of Banana Plantation to Combined Use of Organic and Inorganic Fertilizers
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摘要:目的 探明化肥减量配施有机肥对香蕉土壤细菌群落结构特征的影响。方法 设计5个不同施肥处理:不施肥处理(CK,T1);25%化肥配施有机肥(T2);50%化肥配施有机肥(T3);100%化肥(100% CF,T4)和50%化肥(50% CF,T5)。采用Illumina MiSeq高通量测序平台,对土壤细菌16S rRNA基因保守区进行测序,并对不同施肥处理下土壤细菌群落数量、结构和多样性的差异进行生物信息学分析。结果 T1、T2、T3、T4和T5处理的OTUs数分别是30、33、31、34、31个。不同处理中,优势菌群所占的比例各不相同。T3处理提高了土壤中有益菌变形杆菌门(Proteobacteria)和酸杆菌门(Acidobacteria)的相对丰度。各处理土壤细菌的Shannon指数大小顺序为:T3>T5>T2>T1>T4。和单施50% CF(T5)化肥相比,50% CF配施有机肥处理(T3)提高了土壤细菌多样性。与T5处理相比,T2处理的多样性降低,说明化肥用量过低不利于土壤多样性的提高。T4处理的微生物多样性最低,表明过量的化肥施入降低了土壤微生物多样性。主坐标分析和热图分析结果表明,不同处理细菌群落结构、相对丰度和优势菌群发生了明显的变化。结论 与单施化肥相比,合理的有机无机配施能够提高土壤细菌多样性、改善土壤细菌群落结构。减氮50%配施有机肥(T3)处理不仅减少了氮肥施用量,而且增加了土壤有益细菌的相对丰度和土壤细菌多样性,有利于土壤生物肥力的提高。Abstract:Objective Effects of combined application of organic and chemical fertilizers on the bacterial community in soil of banana plantations were studied.Method Various proportions of chemical fertilizer combined with an organic fertilizer, as well as all or reduced chemical fertilizer, were mixed in the soil from a banana plantation to determine the effect of the applications on the bacterial community in soil. The treatments included the uses of no fertilizer as control (T1), 25% chemical fertilizer (T2), 50% chemical fertilizer (T3), 100% chemical fertilizer (T4), and 50% reduced chemical fertilizer without organic fertilizer (T5). 16S rRNA genes of the bacteria were analyzed by Illumina MiSeq high-throughput sequencing. A bioinformatic analysis was performed to determine the structure, abundance, and diversity of the bacterial communities in soil under treatments.Result The OTUs of the T1, T2, T3, T4, and T5 treatments were 30, 33, 31, 34, and 31, respectively. The proportion of beneficial bacteria in the soils varied by the treatments. The relative abundances of beneficial proteobacteria and acidobacteria were increased by the treatment of T3. The Shannon index of the bacteria in soil under different treatments ranked as T3>T5>T2>T1>T4. In comparison to T5, T3 improved and T2 reduced the soil bacterial diversity indicating a disadvantage of the reduced use of chemical fertilizer. However, the lowest diversity was observed under T4 which showed excessive chemical fertilization to be detrimental, nonetheless. The PCoA and heat map analyses revealed significant changes on the bacterial compositions, relative abundance, and beneficial bacteria in the soil by the treatments.Conclusion Comparing to the use of chemical fertilizer alone, appropriate combination of organic and inorganic fertilizers effectively improved the bacterial diversity and composition in soil. A 50% reduction of chemical fertilizer usage coupled with organic fertilizer (T3) could not only conserve the chemical fertilizer, but also enhance the relative abundances of beneficial bacteria and bacterial diversity resulting in an improved soil fertility.
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0. 引言
【研究意义】施肥是作物增产的主要途径之一。化肥的过量施用导致肥料利用率降低,养分失调和土壤肥力下降,影响农业可持续发展[1-2]。有机肥含有丰富的养分和有机质,它能增强土壤生物学活性,改善土壤理化性状[3-5],提高土壤质量和改善作物品质[6-7]。但是有机肥存在肥效迟缓和养分当季利用率低的缺点。合理的有机无机配施能够兼顾无机肥的速效性和有机肥养分持久性的优点,改善土壤养分的平衡[8-11]。土壤微生物参与土壤有机质的矿化分解和养分的循环转化过程,是土壤养分的储备库和周转库。土壤微生物在改善土壤环境,提高土壤肥力和促进作物生长方面发挥着重要作用。在所有土壤微生物中,细菌所占的丰度最高,参与了土壤中几乎所有的生化反应,其群落结构和多样性是评价土壤质量和肥力的重要指标[12-14]。因此,开展特定区域有机无机配施对土壤微生物生态的影响研究,对确定合理的有机无机配施比例和农业可持续发展,具有重大的现实意义。【前人研究进展】红壤是我国南方的主要土壤类型,处于高温高湿的气候条件之下,土壤质地黏重,有机质含量低,土壤酸性强,养分流失严重。研究表明有机无机配施是提高红壤肥力水平和作物产量的有效措施。吕真真等[15]研究了有机无机配施比例对江西红壤田土壤微生物的影响,结果表明与对照相比,高比例配施有机肥显著提高了土壤细菌的数量。刘淑军等[16]以湖南红壤稻田土壤为研究对象,结果表明与单施无机肥相比,有机无机配施提高了土壤肥力质量指数。然而,孙瑞波等[17]利用454 高通量测序方法对安徽砂姜黑土的研究表明,化肥配施秸秆还田的有机培肥方式并没有缓解化肥单施对土壤细菌所造成的不利影响。虽然近年来我国学者对土壤微生物学特性进行了大量的研究,但由于气候条件、土壤类型和施肥制度的巨大差异,关于有机无机配施对土壤微生物的影响不尽相同[17-18]。高通量测序技术可以对样本中所有细菌群落进行研究,通过对微生物细胞内特定遗传物质的碱基序列进行检测,结合生物信息学分析方法,可以全面、真实地揭示群落的结构和多样性[19-20]。具有高通量、高灵敏度和高准确性的特点。第二代Illumina Miseq测序平台已被广泛用于环境微生物群落结构和多样性研究[21-23]。【本研究切入点】关于采用高能量测序技术探讨有机无机配施对香蕉田土壤微生物群落的影响还有待深入研究。【拟解决的关键问题】采用高通量测序技术,研究不同比例有机无机配施对香蕉田土壤微生物群落丰度、结构和多样性的影响,从土壤微生物生态的角度,探索合理的有机无机配施比例,为减少香蕉田化肥施用量,制定合理的施肥措施和土壤可持续利用提供参考。
1. 材料与方法
1.1 试验地概况
试验在中国热带农业科学院海口市试验基地(N20°05′,E 110°10′)进行。该区属于热带季风气候,年平均温度24 °C,平均降雨量2067 mm。供试土壤类型为热带红壤。试验前土壤0~20 cm 耕层土壤的养分状况为:pH值5.93,有机质含量12.74 g·kg−1,碱解氮含量98.18 mg·kg−1,速效磷含量13.35 mg·kg−1,速效钾含量65.50 mg·kg−1。香蕉品种为巴西蕉(Musa sp., Cavendish group cv. Baxi)。
1.2 试验设计
在香蕉种植上,当地农民习惯的化肥施肥量折算为N、P2O5和K2O为每株香蕉整个生长期N, 400 g;P2O5, 200 g;K2O, 800 g,本试验中记作100% CF。N、P、K肥分别为尿素、过磷酸钙和硫酸钾。所施用的有机肥折算成所含有机质(OM)量计算,每株整个生长期施用750 g OM。
试验共设4个不同施肥处理:(1)不施肥(CK,T1);(2)25%化肥配施有机肥(T2);(3)50%化肥配施有机肥(T3);(4)100%化肥(T4);(5)50%化肥(T5)。每个处理重复3次,随机区组排列。有机肥和化肥混合后施入土壤,30%在壮苗期施入,45%在孕蕾期施入,25%在成熟期施入。管理措施同当地栽培管理。
在收获期最后一次施肥后10 d,采集耕层土样。每个处理重复采集10个点,混匀为1个样品。剔除杂物后保存于−80 ℃冰箱,用于后续分析。
1.3 土壤细菌高通量测序及生物信息学分析
提取土壤微生物总DNA,以细菌保守区通用引物扩增16S rDNA序列,并采用Illumina MiSeq 测序平台对扩增产物进行测序(广州基迪奥公司)。对得到的高通量测序结果,去除序列中的杂质,以97%的序列相似度为标准,将所有序列组成不同的操作分类单元(OTU, operational taxonomic units)。利用Ribosomal Database Project (RDP)平台对OTU进行物种比对,得到OTU所代表的物种。计算丰富度指数Chao,多样性指数Shannon。
以细菌保守区通用引物进行PCR扩增。PCR产物经纯化后构建测序文库,采用Illumina MiSeq 测序平台对扩增产物进行双端测序(广州基迪奥公司)。测序数据经FLASH软件拼接,利用Mothur软件进行序列优化。将97%相似性水平下序列定义为一个OTU(Operational taxonomic units,操作分类单元)。利用Mothur软件以平均邻近聚类算法进行OTU聚类。根据序列组成进行物种注释和分类。计算多样性指数Shannon。利用Excel和SPSS软件进行数据分析,采用Canoco软件进行主坐标分析(Principle coordinate analysis, PCoA)。
2. 结果与分析
2.1 不同处理土壤细菌类群分析
为了研究各处理中的细菌群落组成,以97%的一致性下将序列聚类成OTUs并进行物种注释,绘制Venn图。结果如图1所示,各处理共有的细菌群落数为24个。T1、T2、T3、T4和T5处理的OTUs数分别是30、33、31、34和31个。与不施肥处理(T1)相比,各施肥处理不同程度地增加了细菌种类。
2.2 细菌群落结构分析
将OTU序列与微生物数据库进行比对,获得对应的物种分类信息并绘制细菌门水平群落组成丰度图(图2)。
在细菌门水平,丰度较高的前10个优势菌门分别为变形杆菌门Proteobacteria,放线菌门Actinobacteria,绿弯菌门Chloroflexi,酸杆菌门Acidobacteria,厚壁菌门Firmicutes,浮霉菌门Planctomycetes,芽单胞菌门Gemmatimonadetes,拟杆菌门Bacteroidetes,疣微菌门Verrucomicrobia和糖细菌门Saccharibacteria(表1)。
表 1 不同施肥处理下土壤主要细菌门的相对丰度Table 1. Relative abundances of major bacterial phyla in soil under treatments细菌种类Bacterial species 处理1 T1 处理2 T2 处理3 T3 处理4 T4 处理5 T5 变形杆菌门Proteobacteria 16.65 19.81 20.44 16.26 18.95 放线菌门Actinobacteria 15.78 18.75 16.44 19.09 18.17 绿弯菌门Chloroflexi 16.22 13.94 15.31 16.53 17.25 酸杆菌门Acidobacteria 11.72 12.73 16.09 15.03 13.23 厚壁菌门Firmicutes 14.61 12.14 12.09 12.39 12.64 浮霉菌门Planctomycetes 9.57 9.88 8.14 7.07 7.04 芽单胞菌门Gemmatimonadetes 2.05 2.52 1.90 1.78 2.00 拟杆菌门Bacteroidetes 2.62 2.31 1.23 1.08 1.14 疣微菌门Verrucomicrobia 3.94 1.35 1.03 0.74 0.54 糖细菌门Saccharibacteria 0.23 0.82 0.62 0.98 1.02 在5个不同处理中,这几种优势菌群所占的比例各不相同(表1)。T1处理中比例最高的物种为变形杆菌门Proteobacteria(16.65%),其次为绿弯菌门Chloroflexi(16.22%)和放线菌门Actinobacteria(15.78%)。T2处理中优势菌群所占比例最高的前3类物种分别为变形杆菌门Proteobacteria(19.81%)、放线菌门Actinobacteria(18.75%)和绿弯菌门Chloroflexi(13.94%)。T3处理中前3类优势菌群分别为变形杆菌门Proteobacteria(20.45%),放线菌门Actinobacteria(16.44%)和酸杆菌门Acidobacteria(16.09%)。T4处理中前3类优势菌群分别为放线菌门Actinobacteria(19.09%)、绿弯菌门Chloroflexi(16.53%)和变形杆菌门Proteobacteria(16.26%)。T5处理中前3类优势菌群分别为变形杆菌门Proteobacteria(18.95%),放线菌门Actinobacteria(18.17%)和绿弯菌门Chloroflexi(17.25%)。
与50% CF (T5)和100% CF(T4)相比,在相对丰度大于10%的主要优势细菌中,50% CF配施有机肥(T3)提高了变形杆菌门Proteobacteria和酸杆菌门Acidobacteria的相对丰度。
2.3 不同处理土壤细菌多样性分析
Shannon指数和Simpson指数可以反映物种多样性。由表2可知,Shannon指数的变化趋势为:T3>T5>T2>T1>T4。和单施50% CF (T5)化肥相比,50% CF配施有机肥处理(T3)提高了土壤微生物多样性。然而,25% CF配施有机肥处理(T2)的多样性却较T5处理低,这说明化肥用量过低不利于土壤多样性的提高。100% CF (T4)处理的微生物多样性最低,表明过量的化肥施入降低了土壤微生物多样性。
表 2 不同处理土壤细菌群落多样性指数Table 2. Diversity index of bacteria in soil under treatments处理Treatment Shannon指数Shannon index Simpson指数Simpson index 测序深度指数Sequencing depth index OTU数量OTU number 处理1 T1 9.109 0.993 0.995 2559.000 处理2 T2 9.111 0.996 0.995 2341.333 处理3 T3 9.217 0.996 0.995 2467.000 处理4 T4 8.845 0.996 0.996 2181.667 处理5 T5 9.114 0.996 0.996 2379.333 由此可知,化肥配施有机肥提高了土壤细菌群落的多样性,且适量的化肥有机肥配施更有利于土壤细菌多样性的提高。
2.4 不同处理细菌群落差异分析
为评估不同处理细菌群落间的差异,采用主坐标法在细菌门水平上进行分析。图3表明,不同处理样本分别分布于坐标轴的不同区域,说明不同处理细菌结构之间存在明显差异。100% CF (T4)和50% CF (T5)在坐标轴上的分布较为相似,共同位于横坐标轴的右半轴。对照(T1)和25% CF配施有机肥处理明显与其他处理样本分开,说明与其他处理细菌结构间存在明显差异。
2.5 不同处理土壤细菌组成的比较分析
热图是通过比较不同样品物种丰度的相对大小,利用颜色差异来代表数据矩阵中数值的大小,进而显示不同处理菌群结构的相似点和不同点。结果如图4所示,不同处理菌群中细菌群落丰度的相对大小和优势菌种发生了明显的变化。
从图4可以看出,相比较于其他处理,T1处理的优势菌群主要为厚壁菌门Firmicutes、疣微菌门Verrucomicrobia和硝化螺旋菌门Nitrospirae。T2处理的优势菌群主要为芽单胞菌门Gemmatimonadetes、匿杆菌门Latescibacteria和广古菌门Euryarchaeota。T3处理的优势菌群主要为衣原体门Chlamydiae和细菌类TM6。T4处理的优势菌群主要为蓝细菌Cyanobacteria。T5处理的优势菌群主要为GAL15。
3. 讨论与结论
长期单一的氮肥施用易导致土壤pH值降低和养分的失衡,易引起土壤质量的退化,使土壤微生物向真菌型发展[24]。Zeng等[25]的研究表明化肥配施有机肥可以促进细菌的生长与繁殖。Ye等[26]研究表明,不同类型的有机无机肥配施对土壤有机质含量的贡献不同,相比较于单施化肥,施用有机肥增加了土壤养分,从而为微生物的生长提供了充足的碳源。可见通过调控化肥与有机肥的比例是改善土壤微生物类型,提高土壤肥力的有效措施。王慧颖等[27]研究表明,不同无机有机肥配施比例影响了细菌的群落结构和数量。
本研究表明,与50% CF(T5)处理相比,50% CF配施有机肥(T3)提高了土壤细菌群落的多样性。这可能是由于有机肥含有丰富的营养物质,能为土壤微生物生长提供所需的碳源与氮源,一方面有机肥为细菌的生长提供了营养底物,另一方面改善了施化肥引起的土壤酸化和养分不均衡环境[28-30]。另外,T3处理下变形杆菌门和酸杆菌门的相对丰度最高。变形杆菌门和酸杆菌门是土壤中的有益菌,参与土壤有机物的碳氮循环,从而为土壤提供养分和微生物生长所需能源[31-33]。这说明T3处理有利于土壤中变形杆菌门和酸杆菌门等有益菌的生长,改善了土壤细菌群落结构和组成。25% CF配施有机肥处理(T2)降低了土壤细菌群落的多样性,说明化肥减量过大不利于细菌的生长和土壤微生物生态的改善。因此,在土壤施肥措施上,有机无机配比非常重要。T3处理中变形杆菌门和酸杆菌门等有益菌的相对丰度有所提高,菌群结构得到了改善。岳宏忠等[34]研究发现,微生物有机肥与60%化肥配施后提高了土壤中厚壁菌门和芽孢杆菌纲等有益菌的相对丰度。桑文等[35]研究结果表明施用有机液体肥有利于变形杆菌门和酸杆菌门的生长。这些研究结果与本实验的研究结果一致。
Tang等[36]研究发现,化肥与有机肥以适当比例配施能显著增强土壤细菌的多样性和丰富度指数,本研究结果也证实了这一点。然而魏巍等[37]对东北黑土的研究结果发现,长期施用化肥以及化肥有机肥配施均会显著减低土壤细菌群落的多样性。造成这种差异的原因可能与不同生态区土壤理化性质有关。25%化肥配施有机肥(T2)的土壤细菌多样性(9.111)低于50%化肥处理(9.114),和对照(T1)相似(9.109)。这说明过量的化肥减施不利于土壤细菌多样性的提高。从PCoA分析可知,不同处理在细菌群落分布上存在明显差异。这说明不同施肥处理影响了微生物群落结构。这与前人的研究结果相似[38]。与其他处理相比,100%化肥处理(T4)和50%化肥处理(T5)处理样品的点距离较近,分布相似,说明这2个处理的细菌群落结构差异不明显。
总的来说,化肥配施有机肥提高了土壤微生物活力和多样性,对如何通过施肥管理土壤微生物生态提供了实践经验。后续的工作将重点关注土壤优势菌群的生态功能特征和驱动因素。适量减施化肥配施有机肥能够增加土壤细菌的多样性,增加优势菌群变形杆菌门和酸杆菌门的相对丰度。在减氮50%配施有机肥的情况下,土壤细菌的多样性得到了提高,改善了土壤微生物生态。
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表 1 不同施肥处理下土壤主要细菌门的相对丰度
Table 1 Relative abundances of major bacterial phyla in soil under treatments
细菌种类Bacterial species 处理1 T1 处理2 T2 处理3 T3 处理4 T4 处理5 T5 变形杆菌门Proteobacteria 16.65 19.81 20.44 16.26 18.95 放线菌门Actinobacteria 15.78 18.75 16.44 19.09 18.17 绿弯菌门Chloroflexi 16.22 13.94 15.31 16.53 17.25 酸杆菌门Acidobacteria 11.72 12.73 16.09 15.03 13.23 厚壁菌门Firmicutes 14.61 12.14 12.09 12.39 12.64 浮霉菌门Planctomycetes 9.57 9.88 8.14 7.07 7.04 芽单胞菌门Gemmatimonadetes 2.05 2.52 1.90 1.78 2.00 拟杆菌门Bacteroidetes 2.62 2.31 1.23 1.08 1.14 疣微菌门Verrucomicrobia 3.94 1.35 1.03 0.74 0.54 糖细菌门Saccharibacteria 0.23 0.82 0.62 0.98 1.02 表 2 不同处理土壤细菌群落多样性指数
Table 2 Diversity index of bacteria in soil under treatments
处理Treatment Shannon指数Shannon index Simpson指数Simpson index 测序深度指数Sequencing depth index OTU数量OTU number 处理1 T1 9.109 0.993 0.995 2559.000 处理2 T2 9.111 0.996 0.995 2341.333 处理3 T3 9.217 0.996 0.995 2467.000 处理4 T4 8.845 0.996 0.996 2181.667 处理5 T5 9.114 0.996 0.996 2379.333 -
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