Survival of the fewest: Microbial dormancy and maintenance in marine sediments through deep time

Abstract

Microorganisms buried in marine sediments are known to endure starvation over geologic timescales. However, the mechanisms of how these microorganisms cope with prolonged energy limitation is unknown and therefore yet to be captured in a quantitative framework. Here, we present a novel mathematical model that considers (a) the physiological transitions between the active and dormant states of microorganisms, (b) the varying requirement for maintenance power between these phases, and (c) flexibility in the provenance (i.e., source) of energy from exogenous and endogenous catabolism. The model is applied to sediments underlying the oligotrophic South Pacific Gyre where microorganisms endure ultra‐low fluxes of energy for tens of millions of years. Good fits between model simulations and measurements of cellular carbon and organic carbon concentrations are obtained and are interpreted as follows: (a) the unfavourable microbial habitat in South Pacific Gyre sediments triggers rapid mortality and a transition to dormancy; (b) there is minimal biomass growth, and organic carbon consumption is dominated by catabolism to support maintenance activities rather than new biomass synthesis; (c) the amount of organic carbon that microorganisms consume for maintenance activities is equivalent to approximately 2% of their carbon biomass per year; and (d) microorganisms must rely solely on exogenous rather than endogenous catabolism to persist in South Pacific Gyre sediments over long timescales. This leads us to the conclusion that under oligotrophic conditions, the fitness of an organism is determined by its ability to simply stay alive, rather than to grow. This modelling framework is designed to be flexible for application to other sites and habitats, and thus serves as a new quantitative tool for determining the habitability of and an ultimate limit for life in any environment.

Expanding the diversity of bacterioplankton isolates and modeling isolation efficacy with large scale dilution-to-extinction cultivation

“…These data also match general data indicating prevalent inactivity among aquatic bacterioplankton (104, 111–113). Although labelled uptake methods do not directly measure rates of cell division, the incorporation of these compounds requires active DNA replication or translation, which represent an even more fundamental level of activity than cell division (114).…”

Dormancy dampens the microbial distance-decay relationship

“…In addition, dormancy can influence the commonness and rarity of species in a community while allowing propagules to tolerate conditions that would otherwise prohibit dispersal and colonization [2, 9-11]. Although crucial for understanding the local dynamics of populations and communities [12-14], dormancy is historically neglected when attempting to predict and explain patterns of biodiversity.…”

The Emergence of Life

“…Even supposing the most unlikely event of a sterilizing heat wave through the ocean, the very low thermal conductivity of ocean floor sediments would protect the 'deep biosphere', sparsely populated though it may have been, from heat death (Sleep 2012). We know from medical studies and planetary protection tests how difficult it is to completely eradicate microorganisms once they populate a given habitat, even more so when taking into account the myriad of smaller micro-habitats which could have acted as reservoirs in the event of large extinctions (Bloomfield and Miles 1979;Rummel 2001;Pugel et al 2017;Tirumalai et al 2018aTirumalai et al , 2018bBradley et al 2019).…”