Short-Term Exposure of Paddy Soil Microbial Communities to Salt Stress Triggers Different Transcriptional Responses of Key Taxonomic Groups

Abstract

Soil salinization due to seawater intrusion along coastal areas is an increasing threat to rice cultivation worldwide. While the detrimental impact on rice growth and yield has been thoroughly studied, little is known about how severe salinity affects structure and function of paddy soil microbial communities. Here, we examined their short-term responses to half- and full-strength seawater salinity in controlled laboratory experiments. Slurry microcosms were incubated under anoxic conditions, with rice straw added as carbon source. Stress exposure time was for 2 days after a pre-incubation period of 7 days. Relative to the control, moderate (300 mM NaCl) and high (600 mM NaCl) salt stress suppressed both net consumption of acetate and methane production by 50% and 70%, respectively. Correspondingly, community-wide mRNA expression decreased by 50–65%, with significant changes in relative transcript abundance of family-level groups. mRNA turnover was clearly more responsive to salt stress than rRNA dynamics. Among bacteria, Clostridiaceae were most abundant and the only group whose transcriptional activity was strongly stimulated at 600 mM NaCl. In particular, clostridial mRNA involved in transcription/translation, fermentation, uptake and biosynthesis of compatible solutes, and flagellar motility was significantly enriched in response salt stress. None of the other bacterial groups were able to compete at 600 mM NaCl. Their responses to 300 mM NaCl were more diverse. Lachnospiraceae increased, Ruminococcaceae maintained, and Peptococcaceae, Veillonellaceae, and Syntrophomonadaceae decreased in relative mRNA abundance. Among methanogens, Methanosarcinaceae were most dominant. Relative to other family-level groups, salt stress induced a significant enrichment of transcripts related to the CO dehydrogenase/acetyl-coenzyme A synthase complex, methanogenesis, heat shock, ammonium uptake, and thermosomes, but the absolute abundance of methanosarcinal mRNA decreased. Most strikingly, the transcriptional activity of the Methanocellaceae was completely suppressed already at 300 mM NaCl. Apparently, the key taxonomic groups involved in the methanogenic breakdown of plant polymers significantly differ in their ability to cope with severe salt stress. Presumably, this different ability is directly linked to differences in their genetic potential and metabolic flexibility to reassign available energy resources for cellular adaptation to salt stress.

Resolving Species Level Changes in a Representative Soil Bacterial Community Using Microfluidic Quantitative PCR

“…Moreover, the sets of primers developed here may be useful for studying natural soil community DNA samples (given that our assay targeted common soil species). Although we did not explore this possibility in the current study, the co-extraction of RNA as described in the protocol could be used to link species abundance with community functioning and metabolic activities through quantification of functional genes that provide information on the genetic potential of community members to catalyze certain processes ( Peng et al, 2017 ). Thus, the new approach is suitable to identify general patterns, processes, and functions from a designed consortium or synthetic community that also occur and operate in more complicated ecosystems and can find application to detect members of interest in indigenous communities found soil or other environment harboring microbial life, or even in non-microbial ecosystems ( Prosser et al, 2007 ; O’Malley et al, 2015 ).…”

Novel microbial community composition and carbon biogeochemistry emerge over time following saltwater intrusion in wetlands

“…Although wetlands comprise only a small portion of global landmass, they sequester a disproportionally large amount of organic carbon due to their high primary productivity and the slow rates of decomposition (Bernal & Mitsch, 2012;Mcleod et al, 2011). As sea level continues to rise at an accelerated rate (Church et al, 2013), tidal freshwater wetlands are becoming more susceptible to saltwater intrusion, which may decrease the extent to which these ecosystems sequester carbon (Craft et al, 2009;Herbert et al, 2015) by affecting both plant (Li & Pennings, 2018;Nielsen, Brock, Rees, & Baldwin, 2003) and microbial communities (Morrissey, Gillespie, Morina, & Franklin, 2014;Peng, Wegner, & Liesack, 2017).…”

Effects of forced taxonomic transitions on metabolic composition and function in microbial microcosms

“…Another potential cause for the increased rate similarity could be that in the long term the fluxes in this A B C D poorly mixed system are strongly constrained by boundary conditions and physical transport properties (Louca et al, 2019). A negative effect of salinity on metabolic rates has been observed previously, especially when microorganisms were originally taken from a less saline environment (as in our case) (Wilson et al, 2013;Rath and Rousk, 2015;Peng et al, 2017;Navada et al, 2019;Rath et al, 2019). The effects of salinity are at least partly physiological in nature, with salinity imposing a stress to cells (Rath and Rousk, 2015) that might lead to lower microbial population sizes and generally lower bulk metabolic rates.…”

“…Experiments with microcosms have been particularly useful for disentangling the relationships between environmental conditions, taxonomy, metabolic composition and metabolic function in microbial systems (Widder et al, 2016). Many experiments use chemical treatments to modify microbial taxonomic composition in microcosms, and then examine the effects on a given function (Girvan et al, 2005;Langenheder et al, 2005Langenheder et al, , 2006Peter et al, 2011;Harter et al, 2014;Peng et al, 2017;Rath et al, 2019). Common garden experiments, where microbial communities of different origins are subjected to identical conditions, have also been used to examine the potential effects of origin on metabolic rates (Strickland et al, 2009;Reed and Martiny, 2013;Martiny et al, 2017).…”