Uncovering the biogeographic pattern of the widespread nematode-trapping fungi Arthrobotrys oligospora: watershed is the key

Studies of biogeographic patterns of fungi have long been behind those of plants and animals. The presence of worldwide species, the lack of systematic sampling design and adequate sampling effort, and the lack of research units are responsible for this status. This study investigates the biogeograp...

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Main Authors: Wei Deng, Fa Zhang, Yan-Peng Li, Xin Zhang, Davide Fornacca, Xiao-Yan Yang, Wen Xiao
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1152751/full
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author Wei Deng
Wei Deng
Wei Deng
Fa Zhang
Fa Zhang
Fa Zhang
Yan-Peng Li
Yan-Peng Li
Yan-Peng Li
Yan-Peng Li
Xin Zhang
Xin Zhang
Xin Zhang
Davide Fornacca
Davide Fornacca
Davide Fornacca
Xiao-Yan Yang
Xiao-Yan Yang
Xiao-Yan Yang
Wen Xiao
Wen Xiao
Wen Xiao
Wen Xiao
author_facet Wei Deng
Wei Deng
Wei Deng
Fa Zhang
Fa Zhang
Fa Zhang
Yan-Peng Li
Yan-Peng Li
Yan-Peng Li
Yan-Peng Li
Xin Zhang
Xin Zhang
Xin Zhang
Davide Fornacca
Davide Fornacca
Davide Fornacca
Xiao-Yan Yang
Xiao-Yan Yang
Xiao-Yan Yang
Wen Xiao
Wen Xiao
Wen Xiao
Wen Xiao
author_sort Wei Deng
collection DOAJ
description Studies of biogeographic patterns of fungi have long been behind those of plants and animals. The presence of worldwide species, the lack of systematic sampling design and adequate sampling effort, and the lack of research units are responsible for this status. This study investigates the biogeographical patterns of Arthrobotrys oligospora, the most widespread globally distributed nematode-trapping fungi (NTF), by stratified collecting and analyzing 2,250 samples from 228 sites in Yunnan Province, China. The A. oligospora was isolated, and 149 strains were subjected to ITS, TUB, TEF and RPB2 gene sequencing and multi-gene association phylogeographic analysis. The results show that at population level A. oligospora is randomly distributed throughout Yunnan Province and has no biogeographical distribution pattern. At the genetic level, the phylogenetic tree of A. oligospora diverges into five major evolutionary clades, with a low degree of gene flow between the five clades. However, the correlation between the phylogenetic diversity of A. oligospora and geographical factors was low. There was no clear pattern in the phylogenetic clades distribution of A. oligospora either without dividing the study unit or when the grid was used as the study unit. When watersheds were used as the study unit, 67.4%, 63.3%, 65.9%, 83.3%, and 66.7% of clade 1–5 strains were distributed in the Jinsha river, Red river, Peal river, Lancang river, and Nujiang-Irawaddy river watersheds, respectively. The clades distribution of A. oligospora was highly consistent with the watersheds distribution. Training predictions of the clades distributions using randomly generated polygons were also less accurate than watersheds. These results suggest that watersheds are key to discovering the biogeographic distribution patterns of A. oligospora. The A. oligospora populations are blocked by mountains in the watershed, and gene flow barriers have occurred, which may have resulted in the formation of multiple cryptic species. Watersheds are also ideal for understanding such speciation processes, explaining factors affecting biodiversity distribution and coupling studies of plant and animal and microbial diversity.
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spelling doaj.art-9e10ba58750242b6a529c4c6c30e14bd2023-04-20T05:52:47ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-04-011410.3389/fmicb.2023.11527511152751Uncovering the biogeographic pattern of the widespread nematode-trapping fungi Arthrobotrys oligospora: watershed is the keyWei Deng0Wei Deng1Wei Deng2Fa Zhang3Fa Zhang4Fa Zhang5Yan-Peng Li6Yan-Peng Li7Yan-Peng Li8Yan-Peng Li9Xin Zhang10Xin Zhang11Xin Zhang12Davide Fornacca13Davide Fornacca14Davide Fornacca15Xiao-Yan Yang16Xiao-Yan Yang17Xiao-Yan Yang18Wen Xiao19Wen Xiao20Wen Xiao21Wen Xiao22Institute of Eastern-Himalaya Biodiversity Research, Dali University, Dali, Yunnan, ChinaCollaborative Innovation Center for Biodiversity and Conservation in the Three Parallel Rivers Region of China, Dali, Yunnan, ChinaThe Provincial Innovation Team of Biodiversity Conservation and Utility of the Three Parallel Rivers Region, Dali University, Dali, Yunnan, ChinaInstitute of Eastern-Himalaya Biodiversity Research, Dali University, Dali, Yunnan, ChinaCollaborative Innovation Center for Biodiversity and Conservation in the Three Parallel Rivers Region of China, Dali, Yunnan, ChinaThe Provincial Innovation Team of Biodiversity Conservation and Utility of the Three Parallel Rivers Region, Dali University, Dali, Yunnan, ChinaInstitute of Eastern-Himalaya Biodiversity Research, Dali University, Dali, Yunnan, ChinaCollaborative Innovation Center for Biodiversity and Conservation in the Three Parallel Rivers Region of China, Dali, Yunnan, ChinaThe Provincial Innovation Team of Biodiversity Conservation and Utility of the Three Parallel Rivers Region, Dali University, Dali, Yunnan, ChinaYunling Black-and-White Snub-Nosed Monkey Observation and Research Station of Yunnan Province, Dali, Yunnan, ChinaInstitute of Eastern-Himalaya Biodiversity Research, Dali University, Dali, Yunnan, ChinaCollaborative Innovation Center for Biodiversity and Conservation in the Three Parallel Rivers Region of China, Dali, Yunnan, ChinaThe Provincial Innovation Team of Biodiversity Conservation and Utility of the Three Parallel Rivers Region, Dali University, Dali, Yunnan, ChinaInstitute of Eastern-Himalaya Biodiversity Research, Dali University, Dali, Yunnan, ChinaCollaborative Innovation Center for Biodiversity and Conservation in the Three Parallel Rivers Region of China, Dali, Yunnan, ChinaThe Provincial Innovation Team of Biodiversity Conservation and Utility of the Three Parallel Rivers Region, Dali University, Dali, Yunnan, ChinaInstitute of Eastern-Himalaya Biodiversity Research, Dali University, Dali, Yunnan, ChinaCollaborative Innovation Center for Biodiversity and Conservation in the Three Parallel Rivers Region of China, Dali, Yunnan, ChinaThe Provincial Innovation Team of Biodiversity Conservation and Utility of the Three Parallel Rivers Region, Dali University, Dali, Yunnan, ChinaInstitute of Eastern-Himalaya Biodiversity Research, Dali University, Dali, Yunnan, ChinaCollaborative Innovation Center for Biodiversity and Conservation in the Three Parallel Rivers Region of China, Dali, Yunnan, ChinaThe Provincial Innovation Team of Biodiversity Conservation and Utility of the Three Parallel Rivers Region, Dali University, Dali, Yunnan, ChinaYunling Black-and-White Snub-Nosed Monkey Observation and Research Station of Yunnan Province, Dali, Yunnan, ChinaStudies of biogeographic patterns of fungi have long been behind those of plants and animals. The presence of worldwide species, the lack of systematic sampling design and adequate sampling effort, and the lack of research units are responsible for this status. This study investigates the biogeographical patterns of Arthrobotrys oligospora, the most widespread globally distributed nematode-trapping fungi (NTF), by stratified collecting and analyzing 2,250 samples from 228 sites in Yunnan Province, China. The A. oligospora was isolated, and 149 strains were subjected to ITS, TUB, TEF and RPB2 gene sequencing and multi-gene association phylogeographic analysis. The results show that at population level A. oligospora is randomly distributed throughout Yunnan Province and has no biogeographical distribution pattern. At the genetic level, the phylogenetic tree of A. oligospora diverges into five major evolutionary clades, with a low degree of gene flow between the five clades. However, the correlation between the phylogenetic diversity of A. oligospora and geographical factors was low. There was no clear pattern in the phylogenetic clades distribution of A. oligospora either without dividing the study unit or when the grid was used as the study unit. When watersheds were used as the study unit, 67.4%, 63.3%, 65.9%, 83.3%, and 66.7% of clade 1–5 strains were distributed in the Jinsha river, Red river, Peal river, Lancang river, and Nujiang-Irawaddy river watersheds, respectively. The clades distribution of A. oligospora was highly consistent with the watersheds distribution. Training predictions of the clades distributions using randomly generated polygons were also less accurate than watersheds. These results suggest that watersheds are key to discovering the biogeographic distribution patterns of A. oligospora. The A. oligospora populations are blocked by mountains in the watershed, and gene flow barriers have occurred, which may have resulted in the formation of multiple cryptic species. Watersheds are also ideal for understanding such speciation processes, explaining factors affecting biodiversity distribution and coupling studies of plant and animal and microbial diversity.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1152751/fullresearch unitfungi diversityphylogeographic patternspatial distributionriver
spellingShingle Wei Deng
Wei Deng
Wei Deng
Fa Zhang
Fa Zhang
Fa Zhang
Yan-Peng Li
Yan-Peng Li
Yan-Peng Li
Yan-Peng Li
Xin Zhang
Xin Zhang
Xin Zhang
Davide Fornacca
Davide Fornacca
Davide Fornacca
Xiao-Yan Yang
Xiao-Yan Yang
Xiao-Yan Yang
Wen Xiao
Wen Xiao
Wen Xiao
Wen Xiao
Uncovering the biogeographic pattern of the widespread nematode-trapping fungi Arthrobotrys oligospora: watershed is the key
Frontiers in Microbiology
research unit
fungi diversity
phylogeographic pattern
spatial distribution
river
title Uncovering the biogeographic pattern of the widespread nematode-trapping fungi Arthrobotrys oligospora: watershed is the key
title_full Uncovering the biogeographic pattern of the widespread nematode-trapping fungi Arthrobotrys oligospora: watershed is the key
title_fullStr Uncovering the biogeographic pattern of the widespread nematode-trapping fungi Arthrobotrys oligospora: watershed is the key
title_full_unstemmed Uncovering the biogeographic pattern of the widespread nematode-trapping fungi Arthrobotrys oligospora: watershed is the key
title_short Uncovering the biogeographic pattern of the widespread nematode-trapping fungi Arthrobotrys oligospora: watershed is the key
title_sort uncovering the biogeographic pattern of the widespread nematode trapping fungi arthrobotrys oligospora watershed is the key
topic research unit
fungi diversity
phylogeographic pattern
spatial distribution
river
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1152751/full
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