Effects of Colony Breeding System and Nest Architecture on Soil Microbiome and Fertility in the Fungus-Growing Termite <i>Macrotermes barneyi</i> Light

<i>Macrotermes barneyi</i> is a typical fungus-growing termite that forms both monogynous (single queen) and polygynous (multiple queen) colonies in nature. This species influences the local soil fertility in part by redistributing nutrients across the landscape in its habitats. However,...

Full description

Saved in:
Bibliographic Details
Main Authors: Jiachang Zhou, Wenquan Qin, Yang Zeng, Xin Huang, Jing Yuan, Yuting Yin, Paike Xu, Xiaohong Fan, Runfeng Zhang, Ganghua Li, Yinqi Zhang
Format: Article
Language:English
Published: MDPI AG 2025-04-01
Series:Insects
Subjects:
Online Access:https://www.mdpi.com/2075-4450/16/5/470
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850126842859618304
author Jiachang Zhou
Wenquan Qin
Yang Zeng
Xin Huang
Jing Yuan
Yuting Yin
Paike Xu
Xiaohong Fan
Runfeng Zhang
Ganghua Li
Yinqi Zhang
author_facet Jiachang Zhou
Wenquan Qin
Yang Zeng
Xin Huang
Jing Yuan
Yuting Yin
Paike Xu
Xiaohong Fan
Runfeng Zhang
Ganghua Li
Yinqi Zhang
author_sort Jiachang Zhou
collection DOAJ
description <i>Macrotermes barneyi</i> is a typical fungus-growing termite that forms both monogynous (single queen) and polygynous (multiple queen) colonies in nature. This species influences the local soil fertility in part by redistributing nutrients across the landscape in its habitats. However, how the colony structure of <i>M. barneyi</i> affects nutrient cycling and microbial communities within the nest is not well understood. In this study, we compared the physicochemical properties and microbial communities across nest parts between monogynous and polygynous colonies of <i>M. barneyi</i>. Our results showed that the fungus garden is the most nutrient-rich part of the nest, with higher soil moisture, organic matter, ammonium nitrogen, nitrate nitrogen, available sulfur, available potassium, available silicon, and available boron than other nest parts. Notably, the fungus garden in monogynous colonies had higher nitrate nitrogen, available sulfur, and available silicon than those in the polygynous colonies. The microbial α-diversity in the fungus garden was lower than that in other parts of the nest. β-diversity analysis revealed a clear separation of microbial communities between monogynous and polygynous colonies across nest parts. Furthermore, the relative abundance of functional genes associated with “cell cycle control, cell division, and chromosome partitioning” was higher in the fungus garden of polygynous colonies compared to monogynous colonies. Our results suggest that the fungus garden plays a crucial role in maintaining colony stability in <i>M. barneyi</i> colonies. The rapid depletion of nutrients in the fungus garden to sustain the larger population in polygynous colonies likely influences microbial community dynamics and nutrient cycling.
format Article
id doaj-art-41664e8df22244e2a630e4ffb11c5e9b
institution OA Journals
issn 2075-4450
language English
publishDate 2025-04-01
publisher MDPI AG
record_format Article
series Insects
spelling doaj-art-41664e8df22244e2a630e4ffb11c5e9b2025-08-20T02:33:50ZengMDPI AGInsects2075-44502025-04-0116547010.3390/insects16050470Effects of Colony Breeding System and Nest Architecture on Soil Microbiome and Fertility in the Fungus-Growing Termite <i>Macrotermes barneyi</i> LightJiachang Zhou0Wenquan Qin1Yang Zeng2Xin Huang3Jing Yuan4Yuting Yin5Paike Xu6Xiaohong Fan7Runfeng Zhang8Ganghua Li9Yinqi Zhang10Hubei Key Laboratory of Edible Wild Plants Conservation and Utilization, Hubei Normal University, Huangshi 435002, ChinaHubei Key Laboratory of Edible Wild Plants Conservation and Utilization, Hubei Normal University, Huangshi 435002, ChinaHubei Key Laboratory of Edible Wild Plants Conservation and Utilization, Hubei Normal University, Huangshi 435002, ChinaHubei Key Laboratory of Edible Wild Plants Conservation and Utilization, Hubei Normal University, Huangshi 435002, ChinaHubei Key Laboratory of Edible Wild Plants Conservation and Utilization, Hubei Normal University, Huangshi 435002, ChinaHubei Key Laboratory of Edible Wild Plants Conservation and Utilization, Hubei Normal University, Huangshi 435002, ChinaHubei Key Laboratory of Edible Wild Plants Conservation and Utilization, Hubei Normal University, Huangshi 435002, ChinaHubei Key Laboratory of Edible Wild Plants Conservation and Utilization, Hubei Normal University, Huangshi 435002, ChinaHubei Key Laboratory of Edible Wild Plants Conservation and Utilization, Hubei Normal University, Huangshi 435002, ChinaHubei Key Laboratory of Edible Wild Plants Conservation and Utilization, Hubei Normal University, Huangshi 435002, ChinaKey Laboratory of Termite Control of Ministry of Water Resources, China Institute of Water Resources and Hydropower Research, Beijing 100048, China<i>Macrotermes barneyi</i> is a typical fungus-growing termite that forms both monogynous (single queen) and polygynous (multiple queen) colonies in nature. This species influences the local soil fertility in part by redistributing nutrients across the landscape in its habitats. However, how the colony structure of <i>M. barneyi</i> affects nutrient cycling and microbial communities within the nest is not well understood. In this study, we compared the physicochemical properties and microbial communities across nest parts between monogynous and polygynous colonies of <i>M. barneyi</i>. Our results showed that the fungus garden is the most nutrient-rich part of the nest, with higher soil moisture, organic matter, ammonium nitrogen, nitrate nitrogen, available sulfur, available potassium, available silicon, and available boron than other nest parts. Notably, the fungus garden in monogynous colonies had higher nitrate nitrogen, available sulfur, and available silicon than those in the polygynous colonies. The microbial α-diversity in the fungus garden was lower than that in other parts of the nest. β-diversity analysis revealed a clear separation of microbial communities between monogynous and polygynous colonies across nest parts. Furthermore, the relative abundance of functional genes associated with “cell cycle control, cell division, and chromosome partitioning” was higher in the fungus garden of polygynous colonies compared to monogynous colonies. Our results suggest that the fungus garden plays a crucial role in maintaining colony stability in <i>M. barneyi</i> colonies. The rapid depletion of nutrients in the fungus garden to sustain the larger population in polygynous colonies likely influences microbial community dynamics and nutrient cycling.https://www.mdpi.com/2075-4450/16/5/470polygynousfungus-growing termitesoil fertilitymetagenomics<i>Macrotermes barneyi</i>
spellingShingle Jiachang Zhou
Wenquan Qin
Yang Zeng
Xin Huang
Jing Yuan
Yuting Yin
Paike Xu
Xiaohong Fan
Runfeng Zhang
Ganghua Li
Yinqi Zhang
Effects of Colony Breeding System and Nest Architecture on Soil Microbiome and Fertility in the Fungus-Growing Termite <i>Macrotermes barneyi</i> Light
Insects
polygynous
fungus-growing termite
soil fertility
metagenomics
<i>Macrotermes barneyi</i>
title Effects of Colony Breeding System and Nest Architecture on Soil Microbiome and Fertility in the Fungus-Growing Termite <i>Macrotermes barneyi</i> Light
title_full Effects of Colony Breeding System and Nest Architecture on Soil Microbiome and Fertility in the Fungus-Growing Termite <i>Macrotermes barneyi</i> Light
title_fullStr Effects of Colony Breeding System and Nest Architecture on Soil Microbiome and Fertility in the Fungus-Growing Termite <i>Macrotermes barneyi</i> Light
title_full_unstemmed Effects of Colony Breeding System and Nest Architecture on Soil Microbiome and Fertility in the Fungus-Growing Termite <i>Macrotermes barneyi</i> Light
title_short Effects of Colony Breeding System and Nest Architecture on Soil Microbiome and Fertility in the Fungus-Growing Termite <i>Macrotermes barneyi</i> Light
title_sort effects of colony breeding system and nest architecture on soil microbiome and fertility in the fungus growing termite i macrotermes barneyi i light
topic polygynous
fungus-growing termite
soil fertility
metagenomics
<i>Macrotermes barneyi</i>
url https://www.mdpi.com/2075-4450/16/5/470
work_keys_str_mv AT jiachangzhou effectsofcolonybreedingsystemandnestarchitectureonsoilmicrobiomeandfertilityinthefungusgrowingtermiteimacrotermesbarneyiilight
AT wenquanqin effectsofcolonybreedingsystemandnestarchitectureonsoilmicrobiomeandfertilityinthefungusgrowingtermiteimacrotermesbarneyiilight
AT yangzeng effectsofcolonybreedingsystemandnestarchitectureonsoilmicrobiomeandfertilityinthefungusgrowingtermiteimacrotermesbarneyiilight
AT xinhuang effectsofcolonybreedingsystemandnestarchitectureonsoilmicrobiomeandfertilityinthefungusgrowingtermiteimacrotermesbarneyiilight
AT jingyuan effectsofcolonybreedingsystemandnestarchitectureonsoilmicrobiomeandfertilityinthefungusgrowingtermiteimacrotermesbarneyiilight
AT yutingyin effectsofcolonybreedingsystemandnestarchitectureonsoilmicrobiomeandfertilityinthefungusgrowingtermiteimacrotermesbarneyiilight
AT paikexu effectsofcolonybreedingsystemandnestarchitectureonsoilmicrobiomeandfertilityinthefungusgrowingtermiteimacrotermesbarneyiilight
AT xiaohongfan effectsofcolonybreedingsystemandnestarchitectureonsoilmicrobiomeandfertilityinthefungusgrowingtermiteimacrotermesbarneyiilight
AT runfengzhang effectsofcolonybreedingsystemandnestarchitectureonsoilmicrobiomeandfertilityinthefungusgrowingtermiteimacrotermesbarneyiilight
AT ganghuali effectsofcolonybreedingsystemandnestarchitectureonsoilmicrobiomeandfertilityinthefungusgrowingtermiteimacrotermesbarneyiilight
AT yinqizhang effectsofcolonybreedingsystemandnestarchitectureonsoilmicrobiomeandfertilityinthefungusgrowingtermiteimacrotermesbarneyiilight