Diversity, Persistence and Evolution in Marine Sediments

Publication: ResearchPh.D. thesis

72 % of our planet is covered by saline water, which at its bottom gradually forms a layer of deposited material. This layer of marine sediments harbors active and diverse prokaryotic communities, of which we know little more than just the phylogenetical associ- ation with their often distant, cultured relatives. Because the only inputs are coming from the water column, organisms buried deeper in the sediment live of increasingly recalcitrant organic matter. As a consequence we observe a power-law drop in cell numbers with sed- iment age. When combined with the sulfate reduction rates we can calculate a drop in generation times from tens to thousands years in deepest explored sediments (2.5 km to date). Nevertheless we still find intact cells buried in such an unwelcoming environment. Although some attempts at correlating the geochemical and microbial profiles are being undertaken, most studies treat the whole community as equal, not knowing who and what are the contributions of hydrolyzers, fermenters and terminal oxidizers. In order to address these unknowns I have focused my work on three main aspects of the marine sediments: (i) systematic, analytical description of the microbial communities as they transition from actively growing surface populations to barely dividing subsurface ones; (ii) evolutionary consequences of the prolonged residence in such environments and (iii) inferring function of the dominant groups found in deep sediments.
When the current state of our knowledge on the marine sediments communities was reviewed, it became apparent that there are some global trends in these populations ob- served in deep and shallow, organic rich and poor sediments. We have observed the same, often uncultured, organisms with very similar relative abundance profiles in reviewed sites. In order to better understand this pattern we’ve reviewed the assembly processes that may lead to such situations, keeping in mind the limitations imposed by the environment.We’ve concluded, that due to low energy fluxes, and consequently low number of pos- sible cell divisions, selective survival of pre-adapted populations must be playing the main role in the formation of subseafloor communities.
In order to address the pre-adaptation hypothesis further, we have analyzed the com- munities in multiple stations in Aarhus Bay, and reported findings in line with what we have observed globally. However, having a large detailed study we were also able to trace not only the same phyla but also the same species from the surface down to the deepest sediment. We’ve described these species as ”persister organisms”, and continued the work on describing them further. By using sequencing and bioinformatics tools we were able to target these persisters by obtaining single cell partial genomes and map raw metagenome reads onto them to assess their diversity at di↵erent depths. Using this information we found low mutation rates suggesting, in case of the deepest samples, that only a part of the observed community remains active. No evidence of, with depth, increasingly purifying or more relaxed selection was found, supporting our hypothesis of pre-adaptation of persister organisms to the conditions in the deep biosphere.
The last question that remained unanswered was what are these pre-adaptations that some prokaryota have, that enable them to remain active in the deep biosphere. We’ve ad- dressed that by joining the large volume of information carried by the metagenome with the taxonomical a liations of long fragments and single genomes. The majority of persisters are most likely fermentative organisms, independent of the electron acceptor profiles and geared to degrading complex organic matter by the use of extracellular enzymes. More- over some new functions, unassociated normally with these organisms were found, namely a large diversity of sulfate/sulfite reducers among members of Chloroflexi.
No evidence for selection of repair and recombination functions in the deeper sediment was found, and high number of motility and chemotaxis was detected through the sediment column.
This work casts new light on marine sediment communities, describes their vertical structure and assembly in detail, and pinpoints the properties and identities of the key players. Simultaneously new paths for discussion are opened, about the fraction of active cells, viral impact or the ways of obtaining energy in the deep biosphere.
Original languageEnglish
Number of pages180
StatePublished - 31 Jan 2016

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