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Islands Within Islands: Bacterial Phylogenetic Structure and Consortia in Hawaiian Lava Caves and Fumaroles

Lava caves, tubes, and fumaroles in Hawai‘i present a range of volcanic, oligotrophic environments from different lava flows and host unexpectedly high levels of bacterial diversity. These features provide an opportunity to study the ecological drivers that structure bacterial community diversity an...

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Autores principales: Prescott, Rebecca D., Zamkovaya, Tatyana, Donachie, Stuart P., Northup, Diana E., Medley, Joseph J., Monsalve, Natalia, Saw, Jimmy H., Decho, Alan W., Chain, Patrick S. G., Boston, Penelope J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9349362/
https://www.ncbi.nlm.nih.gov/pubmed/35935195
http://dx.doi.org/10.3389/fmicb.2022.934708
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author Prescott, Rebecca D.
Zamkovaya, Tatyana
Donachie, Stuart P.
Northup, Diana E.
Medley, Joseph J.
Monsalve, Natalia
Saw, Jimmy H.
Decho, Alan W.
Chain, Patrick S. G.
Boston, Penelope J.
author_facet Prescott, Rebecca D.
Zamkovaya, Tatyana
Donachie, Stuart P.
Northup, Diana E.
Medley, Joseph J.
Monsalve, Natalia
Saw, Jimmy H.
Decho, Alan W.
Chain, Patrick S. G.
Boston, Penelope J.
author_sort Prescott, Rebecca D.
collection PubMed
description Lava caves, tubes, and fumaroles in Hawai‘i present a range of volcanic, oligotrophic environments from different lava flows and host unexpectedly high levels of bacterial diversity. These features provide an opportunity to study the ecological drivers that structure bacterial community diversity and assemblies in volcanic ecosystems and compare the older, more stable environments of lava tubes, to the more variable and extreme conditions of younger, geothermally active caves and fumaroles. Using 16S rRNA amplicon-based sequencing methods, we investigated the phylogenetic distinctness and diversity and identified microbial interactions and consortia through co-occurrence networks in 70 samples from lava tubes, geothermal lava caves, and fumaroles on the island of Hawai‘i. Our data illustrate that lava caves and geothermal sites harbor unique microbial communities, with very little overlap between caves or sites. We also found that older lava tubes (500–800 yrs old) hosted greater phylogenetic diversity (Faith's PD) than sites that were either geothermally active or younger (<400 yrs old). Geothermally active sites had a greater number of interactions and complexity than lava tubes. Average phylogenetic distinctness, a measure of the phylogenetic relatedness of a community, was higher than would be expected if communities were structured at random. This suggests that bacterial communities of Hawaiian volcanic environments are phylogenetically over-dispersed and that competitive exclusion is the main driver in structuring these communities. This was supported by network analyses that found that taxa (Class level) co-occurred with more distantly related organisms than close relatives, particularly in geothermal sites. Network “hubs” (taxa of potentially higher ecological importance) were not the most abundant taxa in either geothermal sites or lava tubes and were identified as unknown families or genera of the phyla, Chloroflexi and Acidobacteria. These results highlight the need for further study on the ecological role of microbes in caves through targeted culturing methods, metagenomics, and long-read sequence technologies.
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spelling pubmed-93493622022-08-05 Islands Within Islands: Bacterial Phylogenetic Structure and Consortia in Hawaiian Lava Caves and Fumaroles Prescott, Rebecca D. Zamkovaya, Tatyana Donachie, Stuart P. Northup, Diana E. Medley, Joseph J. Monsalve, Natalia Saw, Jimmy H. Decho, Alan W. Chain, Patrick S. G. Boston, Penelope J. Front Microbiol Microbiology Lava caves, tubes, and fumaroles in Hawai‘i present a range of volcanic, oligotrophic environments from different lava flows and host unexpectedly high levels of bacterial diversity. These features provide an opportunity to study the ecological drivers that structure bacterial community diversity and assemblies in volcanic ecosystems and compare the older, more stable environments of lava tubes, to the more variable and extreme conditions of younger, geothermally active caves and fumaroles. Using 16S rRNA amplicon-based sequencing methods, we investigated the phylogenetic distinctness and diversity and identified microbial interactions and consortia through co-occurrence networks in 70 samples from lava tubes, geothermal lava caves, and fumaroles on the island of Hawai‘i. Our data illustrate that lava caves and geothermal sites harbor unique microbial communities, with very little overlap between caves or sites. We also found that older lava tubes (500–800 yrs old) hosted greater phylogenetic diversity (Faith's PD) than sites that were either geothermally active or younger (<400 yrs old). Geothermally active sites had a greater number of interactions and complexity than lava tubes. Average phylogenetic distinctness, a measure of the phylogenetic relatedness of a community, was higher than would be expected if communities were structured at random. This suggests that bacterial communities of Hawaiian volcanic environments are phylogenetically over-dispersed and that competitive exclusion is the main driver in structuring these communities. This was supported by network analyses that found that taxa (Class level) co-occurred with more distantly related organisms than close relatives, particularly in geothermal sites. Network “hubs” (taxa of potentially higher ecological importance) were not the most abundant taxa in either geothermal sites or lava tubes and were identified as unknown families or genera of the phyla, Chloroflexi and Acidobacteria. These results highlight the need for further study on the ecological role of microbes in caves through targeted culturing methods, metagenomics, and long-read sequence technologies. Frontiers Media S.A. 2022-07-21 /pmc/articles/PMC9349362/ /pubmed/35935195 http://dx.doi.org/10.3389/fmicb.2022.934708 Text en Copyright © 2022 Prescott, Zamkovaya, Donachie, Northup, Medley, Monsalve, Saw, Decho, Chain and Boston. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Prescott, Rebecca D.
Zamkovaya, Tatyana
Donachie, Stuart P.
Northup, Diana E.
Medley, Joseph J.
Monsalve, Natalia
Saw, Jimmy H.
Decho, Alan W.
Chain, Patrick S. G.
Boston, Penelope J.
Islands Within Islands: Bacterial Phylogenetic Structure and Consortia in Hawaiian Lava Caves and Fumaroles
title Islands Within Islands: Bacterial Phylogenetic Structure and Consortia in Hawaiian Lava Caves and Fumaroles
title_full Islands Within Islands: Bacterial Phylogenetic Structure and Consortia in Hawaiian Lava Caves and Fumaroles
title_fullStr Islands Within Islands: Bacterial Phylogenetic Structure and Consortia in Hawaiian Lava Caves and Fumaroles
title_full_unstemmed Islands Within Islands: Bacterial Phylogenetic Structure and Consortia in Hawaiian Lava Caves and Fumaroles
title_short Islands Within Islands: Bacterial Phylogenetic Structure and Consortia in Hawaiian Lava Caves and Fumaroles
title_sort islands within islands: bacterial phylogenetic structure and consortia in hawaiian lava caves and fumaroles
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9349362/
https://www.ncbi.nlm.nih.gov/pubmed/35935195
http://dx.doi.org/10.3389/fmicb.2022.934708
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