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

Abstract

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.

Isolation, antibacterial screening, and identification of bioactive cave dwelling bacteria in Fiji

“…Over 60% of our cultured isolates exhibited antibiotic potential against at least one of the tested pathogenic bacteria. Our study highlights and corroborates the recent report of great microbial diversity in the Oceanic Island caves of Hawaii ( Prescott et al, 2022 ). Our findings are encouraging that many of the bacteria in Oceanic Island caves might be culturable.…”

“…Most bioactive bacteria were identified as genetically diverse Actinomycetes. High diversity of Actinomycetes has also been reported from other cave systems outside of Oceania, and our study adds to the growing appreciation that caves, particularly cave floors and speleothems, harbor a wide range of Actinomycetes and secondary metabolites ( Nimaichand et al, 2015 ; Axenov-Gribanov et al, 2016a ; Maciejewska et al, 2018 ; Hamedi et al, 2019 ; Long et al, 2019 ; Rangseekaew and Pathom-aree, 2019 ; Wiseschart et al, 2019 ; Prescott et al, 2022 ).…”

“…These include absence of light (zero Lux; Ghosh et al, 2016 ), little energy exchange with their external environments ( Kambesis, 2007 ), and many formations of secondary mineral deposits known as speleothems (stalactite and moonmilk in Supplementary Figure S2 ; Bontemps et al, 2021 ). However, cave type, local geology, and surrounding vegetation can all create heterogeneity of mineral and organic surfaces and this can impact cave microhabitats ( Ghosh et al, 2016 , 2020 ; Prescott et al, 2022 ). Specific factors such as pH, temperature, salinity, and resource availability on rock surfaces (e.g., oligotrophic conditions on rock surfaces and limited availability of organic carbon), temperature and humidity can differ within and between caves determine opportunities for microbial growth ( Cuezva et al, 2009 ; Bontemps et al, 2021 ; Iquebal et al, 2021 ).…”

“…Each type of cave has specific properties depending on its heterogeneity of mineral and organic surfaces, and surrounding vegetation. Factors that affect microbial communities include pH, availability of nutrients, total organic carbon (TOC)/liter, low light, temperature, humidity, and geological and biotic histories ( Cuezva et al, 2009 ; Bontemps et al, 2021 ; Iquebal et al, 2021 ; Prescott et al, 2022 ).…”

“…In the last decade, researchers have documented high microbial diversity in caves, including oceanic island caves ( Northup et al, 2011 ; Wall et al, 2015 ; Prescott et al, 2022 ). However, to date, there appears to be no reports of bioactive bacteria isolated from the Island caves of Oceania.…”