Evidence for a growth zone for deep subsurface microbial clades in near-surface anoxic sediments

Global marine sediments harbor a large and highly diverse microbial biosphere, but the mechanism by which this biosphere is established during sediment burial is largely unknown. During burial in marine sediments, concentrations of easily-metabolized organic compounds and total microbial cell abundance decrease steadily. However, it is unknown whether some microbial clades increase with depth, despite the overall trend of abundance decrease. We show total population increases in 38 microbial families over 3 cm of sediment depth in the upper 7.5 cm of White Oak River (WOR) estuary sediments. Clades that increased with depth were more often anaerobic, uncultured, or common in deep marine sediments relative to those that decreased. Minimum turnover times (which are minimum in situ doubling times of growth rates) were estimated to be 2-25 years by combining sedimentation rate with either quantitative PCR (qPCR) or the product of the Fraction Read Abundance of 16S rRNA genes and total Cell counts (FRAxC). Turnover times were within an order of magnitude of each other in two adjacent cores, as well as in two laboratory enrichments of Cape Lookout Bight (CLB), NC, sediments (average difference of 28 {+/-} 19%). qPCR and FRAxC in WOR cores and FRAxC in CLB incubations produced similar turnover times for key deep subsurface uncultured clades Bathyarchaeota (8.7 {+/-} 1.9 years) and Thermoprofundales/MBG-D (4.1 {+/-} 0.7 years). We conclude that common deep subsurface microbial clades experience a narrow zone of growth in shallow sediments, offering an opportunity for natural selection of traits for long-term subsistence after resuspension events. Significance statementThe current dogma is that the deeply-branching uncultured microbes that dominate global marine sediments do not actually increase in population size as they are buried in marine sediments - rather they exist in a sort of prolonged torpor for thousands of years. This is because no evidence has ever been found that these clades actually increase population sizes, or grow, as they are gradually buried. We discovered that they actually do increase population sizes during burial, but only in the upper few centimeters. This changes our dogma about marine sediments as a vast repository of non-growing microbes, to a vast repository of non-growing microbes with a thin and relatively rapid area of growth in the upper 10 centimeters.