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Changes in plant and soil microbial taxonomic and phylogenetic diversity along gradients of land management intensity in Azorean grasslands and forests
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Abstract(s)
Ecossistemas biodiversos, tais como florestas e pastagens, são essenciais para manter serviços ecossistémicos cruciais para a vida no planeta. Esses serviços incluem, entre outros, o sequestro de carbono, fornecimento de água, produção de alimentos e a conservação da biodiversidade, sendo a maioria deles suportados pelo solo.
O habitat do solo suporta plantas, animais e microrganismos e é influenciado pela geologia, clima e vegetação. As atividades humanas impactam significativamente as taxas de erosão do solo, com a agricultura sendo, em larga escala, responsável por essa degradação.
O microbioma do solo é vital para a saúde e fertilidade do solo, influenciando todos os seus processos e as funções do ecossistema que impactam a saúde das plantas e animais terrestres. Além disso, níveis elevados de microrganismos no solo estão associados a um aumento na diversidade à superfície. A metagenómica revolucionou a ecologia microbiana, permitindo um conhecimento sem
precedentes sobre o microbioma do solo, até então desconhecido.
Os Açores, pertencentes à região biogeográfica da Macaronésia, estão entre as regiões mais biodiversas da Europa. No entanto, estas ilhas vulcânicas sofreram uma perda significativa de biodiversidade devido às atividades humanas.
Atualmente, as pastagens ocupam 88% das terras agrícolas produtivas e a principal cultura é o milho forrageiro.
Este estudo tem como objetivo compreender as comunidades microbianas do solo em dois ecossistemas na ilha de São Miguel e estabelecer a referência da sua composição. Este projeto investiga o impacto das florestas naturais e plantadas, bosques exóticos e três tipos de pastagens (seminaturais, permanentes e ressemeadas com milho) nas comunidades fúngicas e bacterianas em 27 locais na ilha para cada ecossistema. Além disso, para as pastagens, as comunidades florísticas também foram estudadas.
Foram colhidas amostras de solo superficial, os parâmetros do solo foram medidos e um inventário da comunidade vegetal foi realizado. O DNA do solo foi extraído e seguidamente sequenciado com recurso à tecnologia Illumina Miseq.
As sequências foram montadas para obter unidades taxonómicas operacionais (OTUs) que representam as comunidades fúngicas e bacterianas. Realizou-se análise de ecologia numérica, máxima verossimilhança e métodos estatísticos Bayesianos, com recurso ao R para analisar os dados.
A altitude, temperatura, precipitação e conteúdo de argila foram significativamente diferentes entre os tipos de floresta. Embora a riqueza de OTUs fúngicas (fOTUs) não tenha sido significativamente diferente, as abundâncias e distribuição de fOTUs variaram (PERMANOVA). Ascomycota foi o filo mais comum entre os 14 obtidos para fOTUs. Um modelo incluindo a densidade do solo, argila, ECEC e EC teve um efeito significativo na riqueza fúngica. Foram encontradas 181 fOTUs indicadoras, pertencentes a cinco filos. As fOTUs indicadoras demonstraram uma clara separação. A riqueza das OTUs bacterianas (bOTUs) diferem significativamente entre florestas exóticas e nativas. A variação de abundâncias e distribuição de bOTUs também foi confirmada por uma PERMANOVA, mas nenhum efeito significativo foi encontrado nos diferentes GLMs explorados. Proteobacteria é o filo dominante entre 26 presentes nos bOTUs. Para estas comunidades, foram encontrados 319 indicadores de 20 filos.
Foram encontradas diferenças significativas entre os tipos de pastagem em vários parâmetros do solo e comunidades de plantas. A pastagem seminatural (SN) apresentou a maior riqueza de espécies de plantas, seguida pela permanente e ressemeada (CR), com diferenças significativas entre as CR e as restantes, tendo-se identificado espécies indicadoras para cada tipo de pastagem. Metade de todas as fOTUs pertenciam a Ascomycota, sem diferença significativa na riqueza.
Um total de 251 fOTUs e 873 bOTUs foram identificados como indicadores para o tipo de pastagem, mostrando uma clara separação entre SN e CR. As comunidades bacterianas consistiram em 41 filos, com Proteobacteria, Acidobacteria, Chloroflexi, Planctomycetes e Patescibacteria a constituir mais de 60%.
Neste estudo, descobrimos que as florestas exóticas têm menor riqueza bacteriana em comparação com as florestas naturais e plantadas, enquanto certos fatores do solo parecem influenciar a riqueza fúngica. Também foram identificadas espécies indicadoras para cada microbioma e tipo de floresta, fornecendo informações sobre o impacto do tipo de floresta nas comunidades
microbianas. Em São Miguel, uma ilha vulcânica com alterações antropogénicas, o microbioma do solo de pastagens e as suas comunidades vegetais variou de acordo com o tipo de pastagem, provavelmente devido a restrições ambientais e à intensidade de gestão. As pastagens permanentes representam um intermédio entre práticas de gestão mais extremas.
Este estudo foi o primeiro a inventariar as comunidades microbianas em três dos tipos mais comuns de pastagens e florestas na ilha de São Miguel. Em geral, mostra diferenças claras no microbioma do solo de pastagens e florestas, provavelmente influenciadas pelas atividades humanas e pela vegetação presente em cada ecossistema. O tipo de solo e o clima também poderão desempenhar um papel importante.
Este estudo destaca o potencial de futuras estratégias de gestão de modo a passar pastagens intensivas para um nível de intensidade médio. Além disso, reforça a importância de controlar espécies invasoras, já que estas têm um impacto negativo no microbioma do solo. Mais estudos são necessários para explorar a relação entre o ambiente, a diversidade vegetal e o microbioma do solo.
ABSTRACT: Biodiverse ecosystems such as forests and grasslands are essential for maintaining environmental services that are crucial for life on our planet. These services include carbon sequestration, water supply, food production, biodiversity conservation, and more, with most of them being supported by soil. The soil habitat is home to plants, animals, microorganisms, and it is shaped by geology, climate, and vegetation. Human activities significantly impact soil erosion rates, with agriculture being a major contributor to this degradation. The soil microbiome is vital for soil health and fertility, influencing all soil processes and ecosystem functions that impact the life of terrestrial plants and animals. Moreover, higher richness of these microorganisms has been associated with increased aboveground diversity. Metagenomics has revolutionized microbial ecology, enabling unprecedented insights to the mostly unknown soil microbiome. The Azores, belonging to the biogeographical region of Macaronesia, are among Europe's most biodiverse regions. However, these volcanic islands have experienced significant biodiversity loss due to human activities. Pasturelands now occupy 88% of agriculturally productive land and the main crop is forage maize. This study aims to understand soil microbial communities in two main ecosystem types on São Miguel Island and establish their baseline composition. It investigates the impact of natural and planted forests, exotic woodlands, and three types of pasturelands (seminatural, permanent, and reseeded with corn) on fungal and bacterial communities across 27 sites on the island for each ecosystem (forests and pastures). Furthermore, for grasslands, plant communities were also studied. Topsoil samples were collected, soil parameters were measured, and a plant community inventory was conducted. The soil DNA was then extracted and sequenced using Illumina Miseq technology. From this sequencing data, operational taxonomic units (OTUs) were assembled to represent the fungal and bacterial communities. Numerical ecology, maximum likelihood, and Bayesian statistical methods were performed using R to analyse the data. Altitude, temperature, precipitation, and silt contents were significantly different between forest types. While the number of fungal OTUs (fOTUs) was not significantly different, the abundances and distribution of fOTUs varied (PERMANOVA). Ascomycota was the most common phylum among the 14 recorded for fOTUs. A model including bulk density, silt, ECEC, and EC had a significant effect on fungal richness. One-hundred-and-one indicative fOTUs were found, belonging to five phyla. Indicative fOTUs were clearly separated. Bacterial OTUs (bOTUs) differ significantly between exotic and native forests. Variation of abundances and distribution of bOTUs was also confirmed by a PERMANOVA, but no significant effects were found in the different GLMs explored. Proteobacteria is the dominant phylum among 26 present in the bOTUs. For this communities 319 indicators from 20 phyla were found. Significant differences were found between pastureland types in terms of various soil parameters and plant communities. Seminatural (SN) had the highest plant species richness, followed by permanent and reseeded (CR), with significant differences between CR and the other two. We also found plant species that were indicative of each pastureland type. Half of all fOTUs belonged to Ascomycota, with no significant difference in richness. A total of 251 fOTUs and 873 bOTUs were identified as indicators for pastureland type, showing clear separation between SN and CR. Bacterial communities consisted of 41 phyla, with Proteobacteria, Acidobacteria, Chloroflexi, Planctomycetes, and Patescibacteria representing more than 60%. In this study, we found that exotic woodlands have less bacterial richness compared to natural and planted forests, while soil factors influence fungal richness. We also identified indicative species for each microbiome and forest type, providing insight into the impact of forest type on microbial communities. In São Miguel, a volcanic island with anthropogenic alterations, the soil microbiota of grasslands and plant communities varied according to pastureland type, likely due to environmental constraints and management intensity. Permanent grasslands represent an intermediate stage between more extreme management practices. This study is the first to inventory microbial communities in three of the mostcommon types of pasturelands and forests on São Miguel Island. Overall, it shows clear differences in the soil microbiome of pasturelands and forests, likely influenced by human activities and vegetation present in each ecosystem. Soil type and climate may also play a role. This study highlights the potential for future management strategies to transition intensive pasturelands to a more medium intensity level. In addition, it reinforces the importance of controlling invasive species as they negatively impact the soil microbiome. Further research is necessary to explore the relationship between environmental, plant diversity and the soil microbiome.
ABSTRACT: Biodiverse ecosystems such as forests and grasslands are essential for maintaining environmental services that are crucial for life on our planet. These services include carbon sequestration, water supply, food production, biodiversity conservation, and more, with most of them being supported by soil. The soil habitat is home to plants, animals, microorganisms, and it is shaped by geology, climate, and vegetation. Human activities significantly impact soil erosion rates, with agriculture being a major contributor to this degradation. The soil microbiome is vital for soil health and fertility, influencing all soil processes and ecosystem functions that impact the life of terrestrial plants and animals. Moreover, higher richness of these microorganisms has been associated with increased aboveground diversity. Metagenomics has revolutionized microbial ecology, enabling unprecedented insights to the mostly unknown soil microbiome. The Azores, belonging to the biogeographical region of Macaronesia, are among Europe's most biodiverse regions. However, these volcanic islands have experienced significant biodiversity loss due to human activities. Pasturelands now occupy 88% of agriculturally productive land and the main crop is forage maize. This study aims to understand soil microbial communities in two main ecosystem types on São Miguel Island and establish their baseline composition. It investigates the impact of natural and planted forests, exotic woodlands, and three types of pasturelands (seminatural, permanent, and reseeded with corn) on fungal and bacterial communities across 27 sites on the island for each ecosystem (forests and pastures). Furthermore, for grasslands, plant communities were also studied. Topsoil samples were collected, soil parameters were measured, and a plant community inventory was conducted. The soil DNA was then extracted and sequenced using Illumina Miseq technology. From this sequencing data, operational taxonomic units (OTUs) were assembled to represent the fungal and bacterial communities. Numerical ecology, maximum likelihood, and Bayesian statistical methods were performed using R to analyse the data. Altitude, temperature, precipitation, and silt contents were significantly different between forest types. While the number of fungal OTUs (fOTUs) was not significantly different, the abundances and distribution of fOTUs varied (PERMANOVA). Ascomycota was the most common phylum among the 14 recorded for fOTUs. A model including bulk density, silt, ECEC, and EC had a significant effect on fungal richness. One-hundred-and-one indicative fOTUs were found, belonging to five phyla. Indicative fOTUs were clearly separated. Bacterial OTUs (bOTUs) differ significantly between exotic and native forests. Variation of abundances and distribution of bOTUs was also confirmed by a PERMANOVA, but no significant effects were found in the different GLMs explored. Proteobacteria is the dominant phylum among 26 present in the bOTUs. For this communities 319 indicators from 20 phyla were found. Significant differences were found between pastureland types in terms of various soil parameters and plant communities. Seminatural (SN) had the highest plant species richness, followed by permanent and reseeded (CR), with significant differences between CR and the other two. We also found plant species that were indicative of each pastureland type. Half of all fOTUs belonged to Ascomycota, with no significant difference in richness. A total of 251 fOTUs and 873 bOTUs were identified as indicators for pastureland type, showing clear separation between SN and CR. Bacterial communities consisted of 41 phyla, with Proteobacteria, Acidobacteria, Chloroflexi, Planctomycetes, and Patescibacteria representing more than 60%. In this study, we found that exotic woodlands have less bacterial richness compared to natural and planted forests, while soil factors influence fungal richness. We also identified indicative species for each microbiome and forest type, providing insight into the impact of forest type on microbial communities. In São Miguel, a volcanic island with anthropogenic alterations, the soil microbiota of grasslands and plant communities varied according to pastureland type, likely due to environmental constraints and management intensity. Permanent grasslands represent an intermediate stage between more extreme management practices. This study is the first to inventory microbial communities in three of the mostcommon types of pasturelands and forests on São Miguel Island. Overall, it shows clear differences in the soil microbiome of pasturelands and forests, likely influenced by human activities and vegetation present in each ecosystem. Soil type and climate may also play a role. This study highlights the potential for future management strategies to transition intensive pasturelands to a more medium intensity level. In addition, it reinforces the importance of controlling invasive species as they negatively impact the soil microbiome. Further research is necessary to explore the relationship between environmental, plant diversity and the soil microbiome.
Description
Tese de Doutoramento, Biologia, 20 de janeiro de 2025, Universidade dos Açores.
Keywords
Solo Metagenómica Microbioma Fungos Bactérias Açores Gestão Florestas Pastagens
Citation
Vieira, Ângela Filipa Almeida Lourenço. (2023). "Changes in plant and soil microbial taxonomic and phylogenetic diversity along gradients of land management intensity in Azorean grasslands and forests
". 135 p. (Tese de Doutoramento em Biologia). Ponta Delgada: Universidade dos Açores, 2023. Disponível em http://hdl.handle.net/10400.3/8605