Marine microbial ecology: Life after volcanic destruction

Destruction of seafloor habitat following a submarine volcanic eruption facilitates construction and recolonization by an intriguing new bacterial species.

A volcanic eruption is as devastating under the sea as it is on land, spewing out molten lava and toxic gas, destroying life in its shadow and disrupting habitats for kilometres in every direction. But out of this destruction comes new land and the opportunity for life to begin again. Writing in Nature Ecology & Evolution1, Danovaro and colleagues explore the biological community established after an eruption of the Tagoro submarine volcano off El Hierro Island, which is part of the Canary Archipelago in the eastern Atlantic Ocean. Armed with remotely operated vehicles (ROV) and the latest microscopic, geochemical, and molecular tools, the authors found what appears to be a new bacterium supporting a novel community of microorganisms and metazoans, flourishing on the volcano-created seafloor.

The volcano erupted between October 2011 and March 2012, disrupting nine square kilometres of the seafloor. Water temperatures and turbidity rose2, dissolved oxygen dropped, and concentrations of hydrogen sulfide, toxic to most organisms, soared, leading to lower primary production and higher fish mortality. When co-author Miquel Canals and his ROV team visited the seafloor in October 2014, they found massive mats of microorganisms covering thousands of square metres around the volcano's cone. They called the most visible microorganism Venus's hair (Fig. 1), perhaps inspired by the long flowing locks of the Roman goddess depicted in Renaissance portraits. Later, genomic data would suggest that the bacterium was related to the sulfur-oxidizing genus, Thioploca.

Figure 1: The Venus's hair habitat.
figure1

Rocks near a submarine volcano were found by Danovaro and colleagues to be covered by a microbial mat dominated by filaments of the Venus's hair bacterium, a H2S oxidizing chemolithoauthotroph, with other bacteria attached to the sheath's outside cover. Panels reproduced with permission from ref. 1, Macmillan Publishers Ltd (Venus's hair illustration); and CRG Marine Geosciences, University of Barcelona (photomicrograph).

Visually striking, the bacterium forms centimetre-long filaments of cells, each 3 to 6 micrometres in diameter, strung together inside a sheath with a width of 36 to 90 micrometres. The ROV team was able to pick out the large filaments for metagenomic analysis. Although dominated by the Venus's hair bacterium, the sample had several genomes (hence the ‘meta’) from sheath-associated bacteria, but one cluster or ‘bin’ of sequences, bin 11 to be exact, stood out; its sequences were most similar to those from the family Thiotrichaceae, in particular Thioploca araucae. The differences are great enough, however, that the authors propose a new genus and species, Thiolava veneris, for the Venus's hair bacterium. It would have been tidier if the authors had been able to do more microscopic analysis with DNA probing to confirm that bin 11 really came from the Venus's hair, but other data point to it being a sulfur-oxidizing bacterium like Thioploca.

Assuming Danovaro and colleagues are right about bin 11, the metagenomic analyses reveal many novel features of the Venus's hair bacterium. As expected it has the sulfur-oxidizing genes characteristic of an organism that gains energy by oxidizing sulfide. This type of bacteria, chemolithoautotrophs, also has genes for fixing CO2 but weirdly the Venus's hair has not one but three CO2 fixation mechanisms. Oxygen is the usual electron acceptor for chemolithoautotrophs, but this bacterium potentially can also use nitrate, which may be more common in the mat where oxygen could become depleted by high metabolic activity. More characteristic of a heterotroph than a chemolithotroph, the bacterium also has genes for using organic material, and Danovaro and colleagues found extracellular enzymatic activity to be high in the mat. Having both chemolithotrophic and heterotrophic capabilities used to be considered unusual, but employing more than one energy-generating mechanism is probably common in the oceans where energy-rich sources are sparse3,4.

In addition to the metagenomic analysis of the filaments, Danovaro and colleagues also looked more deeply at all of the organisms associated with the mat by sequencing taxonomic marker genes retrieved by PCR for both prokaryotes (16S rRNA) and eukaryotes (18S rRNA). In addition to confirming the large difference between the Venus's hair community and vent microorganisms found elsewhere, the 16S rRNA data indicated that the bacteria making up the mat (there were few archaea) were quite different from those in the surrounding seawater. Even more surprising was the diversity of the eukaryotes. These included meiofauna, which are small invertebrates 30 to 1,000 micrometres in size, and larger benthic fauna, probably their larval or juvenile stages. Together the data imply that Venus's hair bacteria, fuelled by hydrogen sulfide still degassing from the volcano, are the system's primary producers at the bottom of a food chain leading eventually to metazoans (Fig. 1). That the energy supporting this habitat is reduced sulfur, not light, is unusual but not unprecedented; an ecosystem based on chemolithoautotrophy was first observed at a hydrothermal vent over 35 years ago5, although the filament metagenome is quite different from hydrothermal vent metagenomes. Novel or not, the Venus's hair mat is certainly an intriguing habitat.

Explorers of new land always have more questions than time and resources for answering them, and that is the case here. One wonders how the barren volcanic rock became covered by a luxurious microbial mat given that the Venus's hair bacterium was not detected in the surrounding seawater and that the Tagoro submarine volcano is far from likely sources of the microorganisms. The observation touches on long-standing questions in microbial biogeography about the dispersal potential of microorganisms and about the role of the ‘rare biosphere’6. Addressing these and other questions would be helped by looking at the succession of microorganisms on the initially virgin volcanic surfaces, starting with colonization by the first microorganism hours after the lava cools. Perhaps work could address even broader questions about where and how a cell first formed to take advantage of geothermal energy7 like microorganisms now do at the Tagoro volcano. Regardless, the Venus's hair community is a fascinating example of a geological force destroying a habitat while also creating a new one where life returns and flourishes.

References

  1. 1

    Danovaro, R. et al. Nat. Ecol. Evol. 1, 0144 (2017)

    Article  Google Scholar 

  2. 2

    Ferrera, I. et al. PLoS ONE 10, e0118136 (2015).

    Article  Google Scholar 

  3. 3

    Swan, B. K. et al. Science 333, 1296–1300 (2011)

    CAS  Article  Google Scholar 

  4. 4

    Moran, M. A. et al. Nature 432, 910–913 (2004)

    CAS  Article  Google Scholar 

  5. 5

    Cavanaugh, C. M., Gardiner, S. L., Jones, M. L., Jannasch, H. W. & Waterbury, J. B. Science 213, 340–342 (1981)

    CAS  Article  Google Scholar 

  6. 6

    PedrósAlió, C. Annu. Rev. Mar. Sci. 4, 449–466 (2012)

    Article  Google Scholar 

  7. 7

    Dodd, M. S. et al. Nature 543, 60–64 (2017)

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to David L. Kirchman.

Ethics declarations

Competing interests

The author declares no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kirchman, D. Marine microbial ecology: Life after volcanic destruction. Nat Ecol Evol 1, 0157 (2017). https://doi.org/10.1038/s41559-017-0157

Download citation

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing