Novel organic compounds in tephra as indicators of current and past microbial activity

The deep biosphere describes any habitat located below the surface of the continents and the bottom of the ocean, and comprises much of Earth's total living biomass. Diverse and mostly uncharacterised microorganisms live in the deep biosphere, potentially playing a role in mediating global biogeochemical processes. Understanding the origin, evolution and significance of this realm is of fundamental importance for elucidating the role of the deep biosphere in Earth's biogeochemistry and understanding how microorganisms thrive in such extreme environments, which in turn may provide insight into life elsewhere in the solar system. Due to the unknown importance the deep biosphere may play on Earth and also in the search for extra-terrestrial life, this realm has received considerable attention in research endeavours over the past three decades. Despite this, it is the most poorly understood ecosystem on Earth.

The International Ocean Discovery Program (IODP) provides access to the deep biosphere. Sediment cores recovered from previous expeditions off the coast of Montserrat (Expedition 340, Site U1396) and the Aleutian Islands (Expedition 323, Site U1339) have been characterised in terms of the organic matter present throughout the sections. These sites comprise both background sediments largely derived from settling of the remains of plankton through the water column (high in carbonate at Site U1396 and silica at U1339) and volcanogenic products. The latter source arises because both sites are proximal to volcanoes, resulting in material from erupted volcanoes being rapidly transported to the oceans. Consistently, the organic material preserved in the volcanic material (termed tephra) is very different from that preserved in the background sediments. Of particular interest within the tephra are a series of amide and sulphonamide compounds (compounds with the functional group -NH2) that are either in much lower abundance or completely absent in the background sediments. These compounds have been hypothesised to originate from microbial activity occurring within the tephra. Microbial colonisation of tephra has been found at other locations where water and tephra are in contact and similar compounds have been suggested to be synthesised by various microorganisms.

Unfortunately, no microbiology studies were conducted at Sites U1339 and U1396, hence the aim of this study is to further test this hypothesis at a new site off the coast of Muroto, Japan. This site has been drilled before and contains significant volumes of tephra. IODP Expedition 370 aims to drill in this region again, specifically to investigate microorganisms within the deep biosphere, making this an ideal location and time to test our hypothesis. Several questions can be addressed with this research:
1) Are there distinct novel organic compounds associated with microbiological activity over the range of temperature and other environmental factors in the sediments?
2) Does the concentration and composition of these compounds vary according to the intensity of microbial activity? If so, can we use them as a proxy measure of activity?
3) Does the concentration and composition of these compounds vary according to the sediment/porewater composition?
4) Do biomarkers persist in sediments that no longer contain microbial activity? If so, can we use them as biomarkers of past microbial activity?

Expedition 370 samples will, for the first time, have well constrained profiles of depth/temperature, microbial lipids and microbial community composition. This presents the opportunity to test our hypothesis and answer the questions outlined in a robust manner, and potentially provide a new suite of biomarkers with which to look for life in extreme environments. Thus, we may be able to use these compounds as tracers of life in extreme/ancient environments such as in the search for life throughout the solar system in areas known to have experienced volcanism (e.g. Mars).

This project will make significant scientific advances towards our understanding of how microbial communities may thrive in extreme environments. It will expand our understanding of extreme environments and how organisms adapt to survive in such environments, and may provide insight into the evolution of ancient life on Earth. Due to the nature of the extreme environments (water-volcano interactivity) this may also inform the search for life elsewhere in our solar system. This project will benefit organic geochemists, geomicrobiologists and may benefit planetary scientists, as outlined in the academic beneficiaries section.

Benefits to: IODP
The proposed research will address three of the proposed challenges in the 2013-2023 IODP Science Plan: challenge 5 'what are the origin, composition and global significance of deep subseafloor communities', challenge 6 'what are the limits of life in the subseafloor realm' and challenge 7 'how sensitive are ecosystems and biodiversity to environmental change?'. This research will contribute to these by characterising and quantifying novel organic markers identified in tephra layers thought to be associated with microbial communities and establish whether these compounds are associated with specific communities dependent on temperature, whether they can be used to measure activity, if there is any selective preservation based on the background sedimenting material and whether these compounds can be used to trace past microbial activity in the deep biosphere. Publication of this research in internationally recognised peer-reviewed journals will highlight the ongoing importance of IODP as a world leader in scientific collaboration and high impact science.

Benefits to: Public
This research will contribute to topical global questions about global geochemical cycles and the limits as life, as well as the search for life throughout the solar system. Integration of this work with other research conducted into the role of the marine diagenesis of tephra and its effect on carbon cycling will allow this work to also inform past and modern carbon cycling, another contemporary subject receiving significant media attention currently. Involvement with University open days and publication of the results in journals accessible to the public will ensure this research is exposed to the public.

Benefits to: Wider scientific community:
This research represents a multidisciplinary effort, and could have relevance to understanding Earth system processes such as global biogeochemical cycling of nutrients, organic matter burial in the deep ocean and in the search for ancient life in extreme environments, both globally and elsewhere in our solar system. To ensure this research reaches as wide an audience as possible collaboration with all Expedition 370 scientists will be established whilst on-board and maintained through regular updates and sharing of data. Findings will be presented at major national and international conferences, with planned conference presentations at Goldschmidt, the American Geophysical Union Fall Meeting, the International Meeting on Organic Geochemistry, and, results-dependent, the International Conference on Paleoceanography.