Chronic exposure to pesticides disrupts the bacterial and fungal co-existence and the cross-kingdom network characteristics of honey bee gut microbiome

被引:16
作者
Al Naggar, Yahya [1 ,2 ]
Wubet, Tesfaye [1 ,3 ]
机构
[1] UFZ Helmholtz Ctr Environm Res, Dept Community Ecol, Theodor Lieser Str 4, D-06120 Halle, Saale, Germany
[2] Tanta Univ, Fac Sci, Zool Dept, Tanta 31527, Egypt
[3] German Ctr Integrat Biodivers Res iDiv, Puschstr 4, D-04103 Leipzig, Germany
关键词
Gut microbiota; Microbes' coexistence; Pesticides; Dysbiosis; Interkingdom network analysis; Honey bees; PATTERNS;
D O I
10.1016/j.scitotenv.2023.167530
中图分类号
X [环境科学、安全科学];
学科分类号
08 ; 0830 ;
摘要
Gut microbiome communities have a significant impact on bee health and disease and have been shown to be shaped by a variety of factors, including exposure to pesticides and inhive chemicals. However, it is unknown whether pesticide exposure affects the coexistence and cross-kingdom network parameters of bee gut micro biome communities because microbes may compete in the gut environment under different stressors. Therefore, we conducted additional analysis of the microbiome data from our previous study in which we discovered that exposure to two novel insecticides flupyradifurone (FPF) and sulfoxaflor (Sulf) or/and a fungicide, azoxystrobin (Azoxy) caused dysbiosis of bee gut microbiota that was associated with an increase in the relative abundance of opportunistic pathogens such as Serratia marcescens. We investigated for the first time the potential cross kingdom fungal-bacterial interactions using co-occurrence pattern correlation and network analysis. We discovered that exposure to FPF or Sulf alone or in combination with Azoxy fungicide influenced the co-existence patterns of fungal and bacterial communities. Significant differences in degree centrality, closeness centrality, and eigenvector centrality distribution indices were also found in single and double-treatment groups compared to controls. The effects of FPF and Sulf alone on cross-kingdom parameters (bacterial to fungal node ratio, degree of centrality, closeness centrality, and eigenvector centrality) were distinct, but this was reversed when they were combined with Azoxy fungicide. The fungal and bacterial hub taxa identified differed, with only a few shared hubs across treatments, suggesting microbial cross-kingdom networks may be disrupted differently under different stressors. Our findings add to our understanding of pesticide effects on the bee gut microbiome and bee health in general, while also emphasizing the importance of cross-kingdom network analysis in future micro biome research.
引用
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页数:8
相关论文
共 45 条
[21]   Gut microbial communities of social bees [J].
Kwong, Waldan K. ;
Moran, Nancy A. .
NATURE REVIEWS MICROBIOLOGY, 2016, 14 (06) :374-384
[22]   Genomics and host specialization of honey bee and bumble bee gut symbionts [J].
Kwong, Waldan K. ;
Engel, Philipp ;
Koch, Hauke ;
Moran, Nancy A. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2014, 111 (31) :11509-11514
[23]   Disentangling Interactions in the Microbiome: A Network Perspective [J].
Layeghifard, Mehdi ;
Hwang, David M. ;
Guttman, David S. .
TRENDS IN MICROBIOLOGY, 2017, 25 (03) :217-228
[24]   Cross-kingdom co-occurrence networks in the plant microbiome: Importance and ecological interpretations [J].
Lee, Kiseok Keith ;
Kim, Hyun ;
Lee, Yong-Hwan .
FRONTIERS IN MICROBIOLOGY, 2022, 13
[25]   Fungi participate in the dysbiosis of gut microbiota in patients with primary sclerosing cholangitis [J].
Lemoinne, Sara ;
Kemgang, Astrid ;
Ben Belkacem, Karima ;
Straube, Marjolene ;
Jegou, Sarah ;
Corpechot, Christophe ;
Chazouilleres, Olivier ;
Housset, Chantal ;
Sokol, Harry ;
Lionel, Arrive ;
Laurent, Beaugerie ;
Anne, Bourrier ;
Marine, Camus ;
ChafaiNajim ;
Edouard, Chambenois ;
ChaputUlriikka ;
Charlotte, Delattre ;
Chloe, Martineau ;
Laurence, Cholley Monnier ;
DeboveClotilde ;
Xavier, Dray ;
Jean-Francois, Flejou ;
Guillaume, Le Gall ;
Nadia, Hoyeau ;
Julien, Kirchgesner ;
Cecilia, Landman ;
LevevreJeremie ;
Philippe, Marteau ;
Isabelle, Nion-Larmurier ;
Violaine, Ozenne ;
Yann, Parc ;
Philippe, Seksik ;
Harry, Sokol ;
Magali, Svrcek .
GUT, 2020, 69 (01) :92-102
[26]   Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China [J].
Ma, Bin ;
Wang, Haizhen ;
Dsouza, Melissa ;
Lou, Jun ;
He, Yan ;
Dai, Zhongmin ;
Brookes, Philip C. ;
Xu, Jianming ;
Gilbert, Jack A. .
ISME JOURNAL, 2016, 10 (08) :1891-1901
[27]   Pesticide exposure and the microbiota-gut-brain axis [J].
Matsuzaki, Rie ;
Gunnigle, Eoin ;
Geissen, Violette ;
Clarke, Gerard ;
Nagpal, Jatin ;
Cryan, John F. .
ISME JOURNAL, 2023, 17 (08) :1153-1166
[28]   Interactions between fungi and bacteria influence microbial community structure in the Megachile rotundata larval gut [J].
McFrederick, Quinn S. ;
Mueller, Ulrich G. ;
James, Rosalind R. .
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 2014, 281 (1779)
[29]   phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data [J].
McMurdie, Paul J. ;
Holmes, Susan .
PLOS ONE, 2013, 8 (04)
[30]   Evolutionary and Ecological Consequences of Gut Microbial Communities [J].
Moran, Nancy A. ;
Ochman, Howard ;
Hammer, Tobin J. .
ANNUAL REVIEW OF ECOLOGY, EVOLUTION, AND SYSTEMATICS, VOL 50, 2019, 50 :451-+