The Early Microbial Colonizers of a Short-Lived Volcanic Island in the Kingdom of Tonga

Nicholas B. Dragone, Kerry Whittaker, Olivia M. Lord, Emily A. Burke, Helen Dufel, Emily Hite, Farley Miller, Gabrielle Page, Dan Slayback, Noah Fierer

The island of Hunga Tonga Hunga Ha'apai (HTHH) in the Kingdom of Tonga was formed by Surtseyan eruptions and persisted for 7 years before being obliterated by a massive volcanic eruption on 15 January 2022. Before it was destroyed, HTHH was an unparalleled natural laboratory to study primary succession on a newly formed landmass. We characterized the microbial communities found on the surface sediments of HTHH using a combination of quantitative PCR, marker gene sequencing, and shotgun metagenomic analyses. Contrary to expectations, photosynthetic cyanobacteria were not detected in these sediments, even though they are typically dominant in the earliest stages of primary succession in other terrestrial environments. Instead, our results suggest that the early sediment communities were composed of a diverse array of bacterial taxa, including trace gas oxidizers, anoxygenic photosynthesizers, and chemolithotrophs capable of metabolizing inorganic sulfur, with these bacteria likely sourced from nearby active geothermal environments. While the destruction of HTHH makes it impossible to revisit the site to conduct in situ metabolic measurements or observe how the microbial communities might have continued to change over time, our results do suggest that the early microbial colonizers have unique origins and metabolic capabilities. IMPORTANCE The volcanic island of Hunga Tonga Hunga Ha'apai in the Kingdom of Tonga represents a very rare example of new island formation and thus a unique opportunity to study how organisms colonize a new landmass. We found that the island was colonized by diverse microbial communities shortly after its formation in 2015, with these microbes likely originating from nearby geothermal environments. Primary succession in this system was distinct from that typically observed in other terrestrial environments, with the early microbial colonizers relying on unique metabolic strategies to survive on the surface of this newly formed island, including the capacity to generate energy via sulfur and trace gas metabolism.