Antarctic rock and soil microbiomes: Shared taxa, selective pressures, and extracellular DNA effects

[Display omitted] •Rock and soil communities select different bacterial communities in Antarctic deserts.•Soils host a greater diversity than rocks.•Many taxa found in soils are supposed to be present in an active state.•Extracellular DNA inflates diversity metrics in DNA-based studies.•Extracellula...

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Published inGeoderma Vol. 446; p. 116918
Main Authors Canini, Fabiana, Adams, Byron J., D'Acqui, Luigi P., D'Alò, Federica, Zucconi, Laura
Format Journal Article
LanguageEnglish
Published Elsevier B.V 01.06.2024
Elsevier
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Abstract [Display omitted] •Rock and soil communities select different bacterial communities in Antarctic deserts.•Soils host a greater diversity than rocks.•Many taxa found in soils are supposed to be present in an active state.•Extracellular DNA inflates diversity metrics in DNA-based studies.•Extracellular DNA affects estimations of the effect of environmental parameters. Highly adapted and often endemic microbial taxa inhabit soils and rocks of extremely cold and dry Antarctic deserts. However, the source populations of these organisms have not yet been clarified. Local hotspots, rather than worldwide wind dispersion, have been described as the primary sources of microbial diversity. In particular, the endolithic niche offers a buffered environment, where layered microbial communities have been described, whose dispersion due to rock fragmentation may influence the diversity and nutrient availability of the surrounding soils. On the other hand, microorganisms thriving in soils could be transported to rock surfaces and colonise them. However, the bacterial taxa that are differentially selected and those exchanged between these two substrata have never been defined before. Additionally, the microorganisms detected in these substrata using DNA-based approaches may not be alive but may correspond to fragments of extracellular DNA originated from dead cells. To identify the taxa that are shared between the two substrata, the selective filters that drive their distributions, and the effects of relic DNA on subsequent interpretations of community structure, colonized rock samples were collected from sandstone outcrops in three localities, as well as soil samples at increasing distances from the outcrops. Homogeneous samples were divided into aliquots, and one of each aliquot was treated for extracellular DNA depletion. Both native and treated samples were screened for their bacterial composition through 16S rRNA gene metabarcoding. The results provide the first demonstration of the strong selection of bacterial communities in rocks and soils, reporting some taxa potentially exchanged between the two substrates. Specifically, genera differentially selected between the two habitats were identified, likely due to their different microenvironmental conditions, such as differences in their thermal regimes. Additionally, extracellular DNA depletion had few effects at the taxonomic level and on the identification of differentially selected genera between the two substrata, but it increased the number of significant correlations of physicochemical variables with the diversity and composition of the soil microbial communities. These findings lead us to the conclusion that, despite the strong selection of the two substrates, there is microbial propagule interchange between soils and rocks in this environment. Extracellular DNA should be carefully considered since it has a significant impact on microbial diversity estimations.
AbstractList [Display omitted] •Rock and soil communities select different bacterial communities in Antarctic deserts.•Soils host a greater diversity than rocks.•Many taxa found in soils are supposed to be present in an active state.•Extracellular DNA inflates diversity metrics in DNA-based studies.•Extracellular DNA affects estimations of the effect of environmental parameters. Highly adapted and often endemic microbial taxa inhabit soils and rocks of extremely cold and dry Antarctic deserts. However, the source populations of these organisms have not yet been clarified. Local hotspots, rather than worldwide wind dispersion, have been described as the primary sources of microbial diversity. In particular, the endolithic niche offers a buffered environment, where layered microbial communities have been described, whose dispersion due to rock fragmentation may influence the diversity and nutrient availability of the surrounding soils. On the other hand, microorganisms thriving in soils could be transported to rock surfaces and colonise them. However, the bacterial taxa that are differentially selected and those exchanged between these two substrata have never been defined before. Additionally, the microorganisms detected in these substrata using DNA-based approaches may not be alive but may correspond to fragments of extracellular DNA originated from dead cells. To identify the taxa that are shared between the two substrata, the selective filters that drive their distributions, and the effects of relic DNA on subsequent interpretations of community structure, colonized rock samples were collected from sandstone outcrops in three localities, as well as soil samples at increasing distances from the outcrops. Homogeneous samples were divided into aliquots, and one of each aliquot was treated for extracellular DNA depletion. Both native and treated samples were screened for their bacterial composition through 16S rRNA gene metabarcoding. The results provide the first demonstration of the strong selection of bacterial communities in rocks and soils, reporting some taxa potentially exchanged between the two substrates. Specifically, genera differentially selected between the two habitats were identified, likely due to their different microenvironmental conditions, such as differences in their thermal regimes. Additionally, extracellular DNA depletion had few effects at the taxonomic level and on the identification of differentially selected genera between the two substrata, but it increased the number of significant correlations of physicochemical variables with the diversity and composition of the soil microbial communities. These findings lead us to the conclusion that, despite the strong selection of the two substrates, there is microbial propagule interchange between soils and rocks in this environment. Extracellular DNA should be carefully considered since it has a significant impact on microbial diversity estimations.
Highly adapted and often endemic microbial taxa inhabit soils and rocks of extremely cold and dry Antarctic deserts. However, the source populations of these organisms have not yet been clarified. Local hotspots, rather than worldwide wind dispersion, have been described as the primary sources of microbial diversity. In particular, the endolithic niche offers a buffered environment, where layered microbial communities have been described, whose dispersion due to rock fragmentation may influence the diversity and nutrient availability of the surrounding soils. On the other hand, microorganisms thriving in soils could be transported to rock surfaces and colonise them. However, the bacterial taxa that are differentially selected and those exchanged between these two substrata have never been defined before. Additionally, the microorganisms detected in these substrata using DNA-based approaches may not be alive but may correspond to fragments of extracellular DNA originated from dead cells. To identify the taxa that are shared between the two substrata, the selective filters that drive their distributions, and the effects of relic DNA on subsequent interpretations of community structure, colonized rock samples were collected from sandstone outcrops in three localities, as well as soil samples at increasing distances from the outcrops. Homogeneous samples were divided into aliquots, and one of each aliquot was treated for extracellular DNA depletion. Both native and treated samples were screened for their bacterial composition through 16S rRNA gene metabarcoding. The results provide the first demonstration of the strong selection of bacterial communities in rocks and soils, reporting some taxa potentially exchanged between the two substrates. Specifically, genera differentially selected between the two habitats were identified, likely due to their different microenvironmental conditions, such as differences in their thermal regimes. Additionally, extracellular DNA depletion had few effects at the taxonomic level and on the identification of differentially selected genera between the two substrata, but it increased the number of significant correlations of physicochemical variables with the diversity and composition of the soil microbial communities. These findings lead us to the conclusion that, despite the strong selection of the two substrates, there is microbial propagule interchange between soils and rocks in this environment. Extracellular DNA should be carefully considered since it has a significant impact on microbial diversity estimations.
ArticleNumber 116918
Author Zucconi, Laura
D'Alò, Federica
Adams, Byron J.
D'Acqui, Luigi P.
Canini, Fabiana
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  surname: Canini
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  givenname: Byron J.
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  surname: Adams
  fullname: Adams, Byron J.
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  givenname: Luigi P.
  surname: D'Acqui
  fullname: D'Acqui, Luigi P.
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  givenname: Federica
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  givenname: Laura
  orcidid: 0000-0001-9793-2303
  surname: Zucconi
  fullname: Zucconi, Laura
  organization: Department of Ecological and Biological Sciences, University of Tuscia, Viterbo, Italy
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Keywords Soil parameters
extracellular DNA
Substratum effect
Antarctic soils and rocks
Endolithic communities
Soil microbiology
Language English
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Snippet [Display omitted] •Rock and soil communities select different bacterial communities in Antarctic deserts.•Soils host a greater diversity than rocks.•Many taxa...
Highly adapted and often endemic microbial taxa inhabit soils and rocks of extremely cold and dry Antarctic deserts. However, the source populations of these...
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StartPage 116918
SubjectTerms Antarctic soils and rocks
Endolithic communities
extracellular DNA
Soil microbiology
Soil parameters
Substratum effect
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Title Antarctic rock and soil microbiomes: Shared taxa, selective pressures, and extracellular DNA effects
URI https://dx.doi.org/10.1016/j.geoderma.2024.116918
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