Life under Nutrient Limitation in Oligotrophic Marine Environments: An Eco/Physiological Perspective of Sphingopyxis alaskensis (formerly Sphingomonas alaskensis)

Abstract

The oceans of the world are nutrient-limited environments that support a dynamic diversity of microbial life. Heterotrophic prokaryotes proliferate in oligotrophic regions and affect nutrient transformation and remineralization thereby impacting directly on the all marine biota. An important challenge in studying the microbial ecology of oligotrophic environments has been the isolation of ecologically important species. This goal has been recognized not only for its relevance in defining the dynamics of community composition, but for enabling physiological studies of competitive species and inferring their impact on the microbial food web. This review describes the successful isolation attempts of the ultramicrobacterium, Sphingopyxis alaskensis (formerly described as Sphingomonas alaskensis) using extinction dilution culturing methods. It then provides a comprehensive perspective of the unique physiological and genetic properties that have been identified that distinguish it from typical copiotrophic species. These properties are described through studies of the growth phase and growth rate control of macromolecular synthesis, stress resistance and global gene expression (proteomics). We also discuss the importance of integrating ecological and physiological approaches for studying microorganisms in marine environments.

The physiology and ecological implications of efficient growth

“…We propose that the maximal growth efficiency of oligotrophs is higher than copiotrophs and that it is reached at a lower concentration of limiting resource. This is supported by evidence from one of the few comparisons of an oligotroph, Sphingopyxis alaskensis, and a copiotroph, Vibrio angustum, under identical conditions (Cavicchioli et al, 2003). The oligotroph had a greater population density at all dilution rates, and thus resource concentrations, measured in the chemostat.…”

Variations in airborne bacterial communities at high altitudes over the Noto Peninsula (Japan) in response to Asian dust events

“…The air samples when the air mass was suspended around Japanese islands, mainly included the members of the classes Alpha-(Phyllobacteriaceae and Methylobacteriaceae), Gamma-, and Betaproteobacteria, which are commonly dominated in phyllosphere (Redford et al, 2010;Fierer and Lennon, 2011) or freshwater environments (Nold and Zwart, 1998). The atmospheric aerosols transported via marine areas include a high relative abundances of marine bacteria belonging to classes Cyanobacteria (Choi and Noh, 2009) and Alphaproteobacteria (Sphingomonadaceae) (Cavicchioli et al, 2003). This study suggested that bacterial compositions in the atmosphere can be used as air mass tracers, which could identify the levels of mixed air masses transported from different sources.…”

“…The Betaproteobacteria sequences in the non-dust samples mainly contained the Oxalobacteraceae and Comamonadaceae families, which are commonly dominate in freshwater environments (Nold and Zwart, 1998) and on plant leaves (Redford et al, 2010). In addition, the class Alphaproteobacteria in the non-dust samples also included marine bacterial sequences belonging to the family Sphingomonadaceae (Cavicchioli et al, 2003). Bacterial populations originating from marine areas are prevalent in cloud droplets (Amato et al, 2007), in air samples collected from the seashores of Europe (Polymenakou et al, 2008), in storming troposphere (DeLeonRodriguez et al, 2013), and at high altitudes in Japanese regions , suggesting that the marine environments represent a major source of bacteria in clouds.…”

The genomic basis of trophic strategy in marine bacteria

“…S. alaskensis RB2256 was isolated by extinction dilution as a numerically abundant member (Ͼ10 5 cells mL Ϫ1 ) of surface waters (10 m depth) in Resurrection Bay, Alaska and the North Sea, and a closely related strain, AF01, was isolated from 350 m deep, oligotrophic ocean waters near Japan (4-6). Oligotrophic traits of S. alaskensis include the ability to grow slowly with a constant maximum specific growth rate (Ͻ0.2 h Ϫ1 ) on low concentrations (nanomolar) of substrates and maintain a relatively small cell volume (Ͻ0.1 m 3 ) and constant cell size in the shift between starvation and growth conditions (6). The small size provides a mechanism for avoidance of predation, and the high surface area-to-volume ratio allows for efficient nutrient acquisition through high-affinity, broad-specificity uptake systems that are predicted to enable S. alaskensis to be able to achieve doubling times typically observed for bacteria in oligotrophic waters (6,7).…”