不同潮位红树植物叶际微生物群落特征及其影响因素

doi:10.17521/cjpe.2025.0421

植物生态学报 ›› 2026, Vol. 50 ›› Issue (4): 987-1002.DOI: 10.17521/cjpe.2025.0421 cstr: 32100.14.cjpe.2025.0421

不同潮位红树植物叶际微生物群落特征及其影响因素

饶朝康¹, 唐亮¹^,²^,^*()

¹ 海南大学生态学院, 保亭森林生态系统海南省野外科学观测研究站, 国家生态质量综合监测站海南热带雨林站(森林), 海口 570228
² 海南大学海南省环南海陆域生物多样性国际联合研究中心, 海口 570228

收稿日期:2025-11-27 接受日期:2026-02-25 出版日期:2026-04-20 发布日期:2026-06-25
通讯作者: ^*唐亮(tangliang@hainanu.edu.cn)
基金资助:
国家自然科学基金(32460303);海南省自然科学基金(623RC460);海南省研究生创新科研课题(Qhys2024-243)

Characteristics and drivers of mangrove phyllosphere microbial communities across different tidal elevations

RAO Chao-Kang¹, TANG Liang¹^,²^,^*()

¹ Hainan Baoting Tropical Forest Ecosystem Observation and Research Station, National Ecological Quality Comprehensive Monitoriong Station: Hainan Tropical Rainforest Station (Forest), School of Ecology, Hainan University, Haikou 570228, China
² Hainan Provincial International Joint Research Center for Land-based Biodiversity Around the South China Sea, Hainan University, Haikou 570228, China

Received:2025-11-27 Accepted:2026-02-25 Online:2026-04-20 Published:2026-06-25
Contact: ^*TANG Liang(tangliang@hainanu.edu.cn)
Supported by:
National Natural Science Foundation of China(32460303);Hainan Provincial Natural Science Foundation of China(623RC460);Hainan Provincial Innovative Research Projects of Postgraduates(Qhys2024-243)

摘要/Abstract

摘要： 叶际微生物在调节植物养分循环及增强宿主逆境适应性方面发挥着关键作用, 然而, 对于沿潮位梯度分布的红树植物, 其叶际微生物群落对潮间带环境梯度的响应特征及驱动机制仍有待深入探究。该研究以海南东寨港国家级自然保护区内低、中、高3个潮位均有分布的红树植物蜡烛果(Aegiceras corniculatum)和海榄雌(Avicennia marina)为对象, 比较不同潮位下的红树植物叶际附生/内生的细菌与真菌群落特征, 解析宿主身份和潮位梯度对群落结构差异的解释度, 并量化环境与叶片理化性状对群落结构的相对贡献。结果表明, 除内生真菌群落在高潮位表现出最高的特有扩增子序列变体(ASV)数外, 其余3类叶际微生物群落均在低潮位具有最多的特有ASV。不同潮位间叶际细菌和真菌的丰富度和多样性存在显著差异, 群落组成主要由假单胞菌门、放线菌门、拟杆菌门、子囊菌门和担子菌门主导。驱动机制分析显示, 宿主身份是驱动细菌群落结构分异的首要因子, 真菌群落结构则受宿主和潮位交互效应显著影响。相关性分析进一步表明, 叶片功能性状(特别是叶全钙和全钾含量)对叶际微生物群落结构的独立解释度显著高于盐度、温度等环境因子; 此外, 属水平优势类群与特定环境及叶片功能指标间, 亦存在显著关联。综上所述, 红树植物叶际微生物群落的构建是宿主性状与潮汐环境共同作用的结果, 宿主特异性的理化性状决定了群落基线特征, 而潮位梯度则通过环境过滤对群落多样性进行次级调节。该研究明确了不同红树植物在应对潮汐生境异质性时的叶际微生物适应策略, 进一步深化了对红树林叶际微生态系统中“宿主-环境-微生物”互作机制的认识。

关键词: 叶际微生物, 红树植物, 潮位梯度, 群落特征, 叶片功能性状

Abstract:

Aims Phyllosphere microorganisms are pivotal in mediating plant nutrient cycling and promoting host stress tolerance. However, for mangrove plants distributed along tidal gradients, the response patterns and driving mechanisms of phyllosphere microbiomes to intertidal environmental gradients remain to be elucidated.

Methods This study focused on two mangrove species, Aegiceras corniculatum and Avicennia marina, distributed along low (LT), middle (MT), and high (HT) tidal elevations in the Dongzhai Harbor National Nature Reserve, Hainan, China. We compared the community characteristics of epiphytic and endophytic bacterial and fungal assemblages in the phyllosphere across different tidal elevations, parsed the explanatory power of host identity and tidal gradients on community structural differences, and quantified the relative contributions of environmental factors versus leaf physicochemical traits to community structure.

Important findings With the exception of endophytic fungi, which exhibited the highest number of unique amplicon sequence variants (ASV) at HT, the other three phyllosphere communities harbored the greatest numbers of unique ASV at LT. Richness and diversity of both bacterial and fungal communities differed significantly among tidal elevations. Community composition was dominated by the bacterial phyla Pseudomonadota, Actinomycetota, and Bacteroidota, and by the fungal phyla Ascomycota and Basidiomycota. Driving mechanism analysis revealed that host identity was the primary driver of bacterial community differentiation, whereas fungal community structure was significantly shaped by the interaction between host identity and tidal elevation. Correlation analyses further indicated that leaf functional traits (particularly total calcium and total potassium contents) explained a significantly larger unique fraction of community variation than environmental factors such as salinity and temperature. Furthermore, dominant genera exhibited significant associations with specific environmental variables and leaf functional traits. Collectively, these results suggest that mangrove phyllosphere microbiome assembly arises from joint effects of host traits and tidal environments: host-specific physicochemical traits determine the baseline characteristics of the community, while the tidal gradient exerts secondary regulation on community diversity through environmental filtering. These findings clarify the phyllosphere microbial adaptation strategies of different mangrove plants in response to tidal habitat heterogeneity and deepen our understanding of the “host-environment-microbe” interaction mechanisms in mangrove phyllosphere microecosystems.

Key words: phyllosphere, mangrove, tidal elevations, community characteristics, leaf functional traits

饶朝康, 唐亮. 不同潮位红树植物叶际微生物群落特征及其影响因素. 植物生态学报, 2026, 50(4): 987-1002. DOI: 10.17521/cjpe.2025.0421

RAO Chao-Kang, TANG Liang. Characteristics and drivers of mangrove phyllosphere microbial communities across different tidal elevations. Chinese Journal of Plant Ecology, 2026, 50(4): 987-1002. DOI: 10.17521/cjpe.2025.0421

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2025.0421

https://www.plant-ecology.com/CN/Y2026/V50/I4/987

图/表 8

图1 不同潮位附生和内生细菌和真菌群落中相对丰度前10的属。A和B分别为附生和内生细菌群落中相对丰度前10的属。C和D分别为附生和内生真菌群落中相对丰度前10的属。LT, 低潮位; MT, 中潮位; HT, 高潮位。

Fig. 1 Relative abundance of the top 10 dominant bacterial and fungal genera in epiphytic and endophytic communities across tidal elevations. A, B, Relative abundance of the top 10 dominant bacterial genera in epiphytic and endophytic communities, respectively. C, D, Relative abundance of the top 10 dominant fungal genera in epiphytic and endophytic communities, respectively. LT, low tidal elevation; MT, middle tidal elevation; HT, high tidal elevation. Uc, unclassified.

图2 不同植物宿主附生和内生细菌和真菌群落中相对丰度前10的属。A和B分别为附生和内生细菌群落中相对丰度前10的属。C和D分别为附生和内生真菌群落中相对丰度前10的属。AC, 蜡烛果; AM, 海榄雌。

Fig. 2 Relative abundance of the top 10 dominant bacterial and fungal genera in epiphytic and endophytic communities across different plant hosts. A, B, Relative abundance of the top 10 dominant bacterial genera in epiphytic and endophytic communities, respectively. C, D, Relative abundance of the top 10 dominant fungal genera in epiphytic and endophytic communities, respectively. AC, Aegiceras corniculatum; AM, Avicennia marina. Uc, unclassified.

图3 红树植物叶际微生物群落在不同潮位和宿主间的α多样性。A-D分别为附生细菌、内生细菌、附生真菌和内生真菌在不同潮位上的Chao1和Shannon-Wienner指数。E-H分别为两种宿主间对应4类群落的Chao1和Shannon-Wienner指数。LT, 低潮位; MT, 中潮位; HT, 高潮位。AC, 蜡烛果; AM, 海榄雌。箱线图上方不同小写字母表示组间差异显著(p < 0.05)。

Fig. 3 Alpha diversity of mangrove phyllosphere microbial communities across tidal elevations and host plants. A-D, Chao1 richness index and Shannon-Wienner diversity index across the three tidal elevations for epiphytic bacteria, endophytic bacteria, epiphytic fungi, and endophytic fungi, respectively. E-H, The corresponding Chao1 and Shannon-Wienner indices between the two host species for the four microbial categories. LT, low tidal elevations; MT, middle tidal elevations; HT, high tidal elevations. AC, Aegiceras corniculatum; AM, Avicennia marina. Different lowercase letters above the box plots denote a statistically significant difference between groups (p < 0.05).

图4 不同潮位和宿主对叶际微生物群落结构的影响。LT, 低潮位; MT, 中潮位; HT, 高潮位。AC, 蜡烛果; AM, 海榄雌。S, 宿主效应, T, 潮位梯度; S × T, 二者的交互作用。PCoA, 主坐标分析。

Fig. 4 Impact of tidal elevation and host species on phyllosphere microbial community structure. LT, low tidal elevations; MT, middle tidal elevations; HT, high tidal elevations. AC, Aegiceras corniculatum; AM, Avicennia marina. The analysis elucidates the effects of host species (S), tidal gradient (T), and their interactive effect (S × T) on the community structure. PCoA, principal coordinates analysis.

表1 在物种和潮位分层条件下红树植物叶际微生物群落结构的PERMANOVA结果

Table 1 PERMANOVA results for mangrove phyllosphere microbial community structure under hierarchical partitioning of host species and tidal elevation

对照组 Control group	df	细菌 Bacteria				真菌 Fungi
		叶表 Epiphytic		叶内 Endophytic		叶表 Epiphytic		叶内 Endophytic
		R²	p	R²	p	R²	p	R²	p
Species = AC:Tidal	2	0.800	0.007	0.420	0.012	0.622	0.012	0.635	0.007
Species = AM:Tidal	2	0.385	0.043	0.327	0.079	0.307	0.145	0.606	0.007
Tidal = LT:Species	5	0.725	0.100	0.485	0.100	0.327	0.100	0.579	0.100
Tidal = MT:Species	5	0.840	0.100	0.684	0.100	0.726	0.100	0.901	0.100
Tidal = HT:Species	5	0.836	0.100	0.674	0.100	0.416	0.100	0.497	0.100

表2 不同潮位红树植物的环境因子与叶片理化性状(平均值±标准差)

Table 2 Environmental and leaf physicochemical factors of mangrove at different tidal levels (mean ± SD)

物种 Species	变量 Variable	低潮位 LT	中潮位 MT	高潮位 HT
蜡烛果 Aegiceras corniculatum	Sal	19.000 ± 0.265^a	17.967 ± 0.473^b	16.033 ± 0.379^c
	Tem	20.333 ± 1.197^a	20.253 ± 1.991^a	22.467 ± 0.092^a
	Rh	66.437 ± 10.096^a	71.273 ± 8.492^a	64.193 ± 0.705^a
	pH	6.877 ± 0.339^a	6.407 ± 0.360^a	6.063 ± 0.332^a
	LWC	0.317 ± 0.006^a	0.337 ± 0.006^a	0.377 ± 0.055^a
	TK	8.640 ± 0.553^a	8.037 ± 0.391^a	8.507 ± 1.308^a
	TN	17.887 ± 0.498^a	15.857 ± 0.552^ab	15.533 ± 1.296^b
	TP	2.673 ± 0.150^a	2.180 ± 0.070^b	2.307 ± 0.172^b
	Ca	2.963 ± 0.693^a	2.570 ± 0.104^ab	1.733 ± 0.155^b
	Mg	6.203 ± 0.938^a	6.413 ± 0.397^a	3.940 ± 0.295^b
海榄雌 Avicennia marina	Sal	19.500 ± 0.300^a	18.467 ± 0.777^a	15.200 ± 1.153^b
	Tem	20.350 ± 1.225^a	20.737 ± 1.225^a	22.467 ± 0.092^a
	Rh	66.380 ± 10.192^a	68.940 ± 4.664^a	64.193 ± 0.705^a
	pH	6.707 ± 0.552^a	6.107 ± 0.199^a	5.860 ± 0.265^a
	LWC	0.407 ± 0.029^a	0.383 ± 0.012^a	0.390 ± 0.010^a
	TK	3.930 ± 0.352^a	3.890 ± 0.210^a	3.697 ± 0.338^a
	TN	9.200 ± 0.292^a	10.107 ± 0.301^a	9.173 ± 0.751^a
	TP	0.970 ± 0.101^a	1.093 ± 0.035^a	1.090 ± 0.110^a
	Ca	3.527 ± 0.235^a	3.553 ± 0.185^a	3.703 ± 0.454^a
	Mg	3.753 ± 0.662^a	4.917 ± 0.476^a	5.113 ± 0.870^a

图5 微生物群落组成(ASV水平)与环境指标和叶片理化指标的典范对应分析(CCA)和层次分割分析(HPA)。LT, 低潮位; MT, 中潮位; HT, 高潮位。DCA1, 去趋势对应分析第一轴梯度长度值。Ca, 叶全钙含量; LWC, 叶片含水率; Mg, 叶全镁含量; pH, 酸碱度; Rh, 相对湿度; Sal, 盐度; Tem, 气温; TK, 叶全钾含量; TN, 叶全氮含量; TP, 叶全磷含量。

Fig. 5 Canonical correspondence analysis (CCA) and hierarchical partitioning analysis (HPA) of microbial community composition (at the ASV level) with environmental factors and leaf physical and chemical properties. LT, low tidal elevation; MT, middle tidal elevation; HT, high tidal elevation. DCA1, the gradient length value of the first axis of detrended correspondence analysis. Ca, leaf total calcium content; LWC, leaf water content; Mg, leaf total magnesium content; pH, acidity and alkalinity; Rh, relative humidity; Sal, salinity; Tem, air temperature; TK, leaf total potassium content; TN, leaf total nitrogen content; TP, leaf total phosphorus content.

图6 叶际微生物前10优势属与环境指标和叶片理化指标的冗余分析(RDA)。A和B为附生细菌和内生细菌。C和D为附生真菌和内生真菌。LT, 低潮位; MT, 中潮位; HT, 高潮位。AC, 蜡烛果; AM, 海榄雌。DCA1, 去趋势对应分析第一轴梯度长度值。Ca, 叶全钙含量; LWC, 叶片含水率; Mg, 叶全镁含量; pH, 酸碱度; Rh, 相对湿度; Sal, 盐度; Tem, 气温; TK, 叶全钾含量; TN, 叶全氮含量; TP, 叶全磷含量。

Fig. 6 Redundancy analysis (RDA) of the top 10 dominant genera of phyllosphere microorganisms with environmental indicators and leaf physicochemical indicators. A, B, Epiphytic bacteria and endophytic bacteria, respectively. C, D, Epiphytic fungi and endophytic fungi, respectively. LT, low tidal elevation; MT, middle tidal elevation; HT, high tidal elevation. AC, Aegiceras corniculatum; AM, Avicennia marina. DCA1, The gradient length value of the first axis of detrended correspondence analysis. Ca, leaf total calcium content; LWC, leaf water content; Mg, leaf total magnesium content; pH, acidity and alkalinity; Rh, relative humidity; Sal, salinity; Tem, air temperature; TK, leaf total potassium content; TN, leaf total nitrogen content; TP, leaf total phosphorus content.

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不同潮位红树植物叶际微生物群落特征及其影响因素

Characteristics and drivers of mangrove phyllosphere microbial communities across different tidal elevations

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