Exploring the Influence of Ecological Niches and Hologenome Dynamics on the Growth of <i>Encephalartos villosus</i> in Scarp Forests

Information on how bacteria in plants and soil, along with extracellular enzymes, affect nutrient cycling in <i>Encephalartos villosus</i> growing in phosphorus deficient and acidic scarp forests is lacking. Bacteria in coralloid roots, rhizosphere, and non-rhizosphere soils were isolate...

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Main Authors: Nqobile Motsomane, Terence N. Suinyuy, María A. Pérez-Fernández, Anathi Magadlela
Format: Article
Language:English
Published: MDPI AG 2024-01-01
Series:Soil Systems
Subjects:
Online Access:https://www.mdpi.com/2571-8789/8/1/21
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author Nqobile Motsomane
Terence N. Suinyuy
María A. Pérez-Fernández
Anathi Magadlela
author_facet Nqobile Motsomane
Terence N. Suinyuy
María A. Pérez-Fernández
Anathi Magadlela
author_sort Nqobile Motsomane
collection DOAJ
description Information on how bacteria in plants and soil, along with extracellular enzymes, affect nutrient cycling in <i>Encephalartos villosus</i> growing in phosphorus deficient and acidic scarp forests is lacking. Bacteria in coralloid roots, rhizosphere, and non-rhizosphere soils were isolated to determine the potential role of soil bacterial communities and their associated enzyme activities in nutrient contributions in rhizosphere and non-rhizosphere soils. The role of soil characteristics and associated bacteria on <i>E. villosus</i> nutrition and nitrogen source reliance was investigated. <i>Encephalartos villosus</i> leaves, coralloid roots, rhizosphere, and non-rhizosphere soils were collected at two scarp forests. Leaf nutrition, nitrogen source reliance, soil nutrition, and extracellular enzyme activities were assayed. A phylogenetic approach was used to determine the evolutionary relationship between identified bacterial nucleotide sequences. The clustering pattern of isolated bacterial strains was primarily dictated by the ecological niches from which they originated (rhizosphere soil, non-rhizosphere soil, and coralloid roots), thus indicating that host-microbe interactions may be a key driver of this pattern, in line with the hologenome theory. There were insignificant differences in the phosphorus and nitrogen cycling enzyme activities in <i>E. villosus</i> rhizosphere and non-rhizosphere soils in both localities. Significantly positive correlations were recorded between nitrogen and phosphorus cycling enzymes and phosphorus and nitrogen concentrations in rhizosphere and non-rhizosphere soils. Additionally, more than 70% of the leaf nitrogen was derived from the atmosphere. This study challenged the conventional expectation that environmental filters alone dictate microbial community composition in similar habitats and revealed that host-microbe interactions, as proposed by the hologenome theory, are significant drivers of microbial community structuring. The isolated bacteria and their plant growth promoting traits play a role in <i>E. villosus</i> nutrition and nitrogen source reliance and secrete nutrient cycling enzymes that promote nutrient availability in rhizosphere and non-rhizosphere soils.
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spelling doaj.art-b687ce59c1d54e45a24cbb2c717eb5952024-03-27T14:04:51ZengMDPI AGSoil Systems2571-87892024-01-01812110.3390/soilsystems8010021Exploring the Influence of Ecological Niches and Hologenome Dynamics on the Growth of <i>Encephalartos villosus</i> in Scarp ForestsNqobile Motsomane0Terence N. Suinyuy1María A. Pérez-Fernández2Anathi Magadlela3School of Life Sciences, College of Agriculture, Engineering and Science, University of KwaZulu-Natal (Westville Campus), Private Bag X54001, Durban 4000, South AfricaSchool of Biology and Environmental Sciences, University of Mpumalanga (Mbombela Campus), Private Bag X11283, Mbombela 1200, South AfricaDepartment of Physical, Chemical and Natural Systems, Universidad Pablo de Olavide, Carretera de Utrera Km 1, 41013 Seville, SpainSchool of Life Sciences, College of Agriculture, Engineering and Science, University of KwaZulu-Natal (Westville Campus), Private Bag X54001, Durban 4000, South AfricaInformation on how bacteria in plants and soil, along with extracellular enzymes, affect nutrient cycling in <i>Encephalartos villosus</i> growing in phosphorus deficient and acidic scarp forests is lacking. Bacteria in coralloid roots, rhizosphere, and non-rhizosphere soils were isolated to determine the potential role of soil bacterial communities and their associated enzyme activities in nutrient contributions in rhizosphere and non-rhizosphere soils. The role of soil characteristics and associated bacteria on <i>E. villosus</i> nutrition and nitrogen source reliance was investigated. <i>Encephalartos villosus</i> leaves, coralloid roots, rhizosphere, and non-rhizosphere soils were collected at two scarp forests. Leaf nutrition, nitrogen source reliance, soil nutrition, and extracellular enzyme activities were assayed. A phylogenetic approach was used to determine the evolutionary relationship between identified bacterial nucleotide sequences. The clustering pattern of isolated bacterial strains was primarily dictated by the ecological niches from which they originated (rhizosphere soil, non-rhizosphere soil, and coralloid roots), thus indicating that host-microbe interactions may be a key driver of this pattern, in line with the hologenome theory. There were insignificant differences in the phosphorus and nitrogen cycling enzyme activities in <i>E. villosus</i> rhizosphere and non-rhizosphere soils in both localities. Significantly positive correlations were recorded between nitrogen and phosphorus cycling enzymes and phosphorus and nitrogen concentrations in rhizosphere and non-rhizosphere soils. Additionally, more than 70% of the leaf nitrogen was derived from the atmosphere. This study challenged the conventional expectation that environmental filters alone dictate microbial community composition in similar habitats and revealed that host-microbe interactions, as proposed by the hologenome theory, are significant drivers of microbial community structuring. The isolated bacteria and their plant growth promoting traits play a role in <i>E. villosus</i> nutrition and nitrogen source reliance and secrete nutrient cycling enzymes that promote nutrient availability in rhizosphere and non-rhizosphere soils.https://www.mdpi.com/2571-8789/8/1/21cycad-microbe symbiosisphosphorus deficient soilsbiological nitrogen fixation
spellingShingle Nqobile Motsomane
Terence N. Suinyuy
María A. Pérez-Fernández
Anathi Magadlela
Exploring the Influence of Ecological Niches and Hologenome Dynamics on the Growth of <i>Encephalartos villosus</i> in Scarp Forests
Soil Systems
cycad-microbe symbiosis
phosphorus deficient soils
biological nitrogen fixation
title Exploring the Influence of Ecological Niches and Hologenome Dynamics on the Growth of <i>Encephalartos villosus</i> in Scarp Forests
title_full Exploring the Influence of Ecological Niches and Hologenome Dynamics on the Growth of <i>Encephalartos villosus</i> in Scarp Forests
title_fullStr Exploring the Influence of Ecological Niches and Hologenome Dynamics on the Growth of <i>Encephalartos villosus</i> in Scarp Forests
title_full_unstemmed Exploring the Influence of Ecological Niches and Hologenome Dynamics on the Growth of <i>Encephalartos villosus</i> in Scarp Forests
title_short Exploring the Influence of Ecological Niches and Hologenome Dynamics on the Growth of <i>Encephalartos villosus</i> in Scarp Forests
title_sort exploring the influence of ecological niches and hologenome dynamics on the growth of i encephalartos villosus i in scarp forests
topic cycad-microbe symbiosis
phosphorus deficient soils
biological nitrogen fixation
url https://www.mdpi.com/2571-8789/8/1/21
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