Low Temperature and High Hydrostatic Pressure Have Compounding Negative Effects on Marine Microbial Motility

Abstract

ABSTRACTApproximately three fourths of all pelagic marine prokaryotes live in the deep-sea, an environment characterized by low temperature and high hydrostatic pressure. Within deep-sea environments labile organic matter is often scarce and motility can serve as a competitive advantage for microorganisms. Experimental work with a handful of species suggests motility is one of the most temperature- and pressure-sensitive cellular processes, however the combined effects of temperature and pressure together have yet to be investigated in detail. Here we employed growth-dependent motility agar assays and growth-independent microscopy assays to assess how changes in these two physical factors impact motility both individually and in combination, using ecologically relevant model organisms from the cosmopolitan generaHalomonas, Alcanivorax, andMarinobacter. At pressures equivalent to bathyal and abyssal depths, changes in temperature from 30°C to 4°C (motility assays) or 23°C to 7°C (microscopy assays) had a greater influence on motility than pressure. In addition, low-temperature and high-pressure impacts were additive. Exposure to high pressure had varying degrees of effect on flagellar function, depending on the strain and the magnitude of the pressure. These ranged from short-term impacts that were quickly reversible to long-term impacts that were detrimental to the function of the flagellum, leading to complete loss of motility. These findings highlight the sensitivity of deep-sea bacterial motility systems to combined temperature/pressure conditions, phenotypes that will contribute to the modulation of diverse microbial activities at depth.IMPORTANCEMicroorganisms perform critical functions in biogeochemical cycles at depth, as well as likely modulating the carbon sequestration potential of the deep ocean. However, their activities under in situ conditions are poorly constrained. One aspect of microbial activity is motility, generally mediated by the energy-consuming rotation of one or more flagellar filaments that enables swimming behavior. This provides a competitive advantage for microbes in the environment, such as by enhancing nutrient acquisition. Here we report on culture-based and microscopy-based analyses of pressure-temperature (P-T) effects on the motility of three ecologically relevant marine microbes. The results in all cases indicate that high pressure and low temperature exert compounding inhibitory effects. This argues for the need for further investigations into P-T effects on deep-sea microbial processes.