Characterization and growth response to temperature and salinity of psychrophilic, halotolerant Chlamydomonas sp. ARC isolated from Chukchi Sea ice

Abstract

Sea ice provides a habitat for a diverse community of microorganisms, which comprise a substantial portion of primary production in ice-covered seas. Organisms immured in sea ice have to withstand strong changes in temperature and salinity. We report on the growth rate response to salinity and temperature of the chlorophyte Chlamydomonas sp. ARC, isolated from land-fast sea ice in the Chukchi Sea, Alaska. We found it to be a euryhaline psychrophile capable of growth at temperatures as low as -5°C and at salinities from 2.5 to 100 ‰. The maximum growth rate of 0.41 d -1 (± 0.027) was found at 5°C and a salinity of 30 ‰. The salinity growth range of this organism indicates that it is well adapted to the variable salinity environment associated with brine channels in sea ice, as well as the hypotonic conditions associated with melting ice. Based upon morphology and molecular phylogenetic reconstructions using the 18S ribosomal ribonucleic acid (rRNA) gene and the ribulose 1, 5-bisphosphate carboxylase/oxygenase large subunit (rbcL) gene, this Arctic Chlamydomonas falls into a distinct clade containing other as yet unassigned psychrophilic Chlamydomonas strains isolated from Arctic and Antarctic environments, pointing to a bi-polar distribution of this clade. It is also very closely related to the brackish water mesophile Chlamydomonas kuwadae Gerloff, and is capable of growth above the psychrophilic range in low-salinity medium, indicating that it may represent an intermediate between mesophilic and psychrophilic lifestyles.KEY WORDS: Chlamydomonas · Chlorophyta · Arctic sea ice · Chukchi Sea · Psychrophile · Euryhaline · Phylogeny 354: 107-117, 2008 temperatures, ice algae growing in the brine channels need to be tolerant of widely varying salinities. Resale or republication not permitted without written consent of the publisherMar Ecol Prog SerIn physiological studies testing the adaptation of Antarctic ice algae to low temperature and high salinity, Bartsch (1989) found that cell division was observed at temperatures as cold as -5.5°C and a salinity of 90 ‰. Aletsee & Jahnke (1992) reported growth of the marine diatoms Nitzschia frigida Grunow and Thalassiosira antarctica Comber at temperatures as low as -8 and -6°C and at salinities of 145 and 109 ‰, respectively. In general, sea-ice diatoms are often euryhaline and thrive in conditions from 10 to 60 ‰ (Grant & Horner 1976).Diatoms have been the focus of most studies on seaice algae, because they are considered the most abundant phototrophs in sea ice (Horner 1985, Lizotte 2003. Green algae are usually a relatively minor component, but the chlorophyte Chlamydomonas spp. has been found repeatedly in Arctic sea ice (see 'Discussion'). Chlamydomonas species may play a disproportionably large role in the initial colonization of sea ice. Weissenberger (1998) found Chlamydomonas sp. to dominate newly formed ice for the first 3 mo in a tank experiment inoculated with an enrichment culture from sea-ice brine. Despite their ubiquity in Arctic sea ice, most ...

Generic and species concepts inMicroglena(previously theChlamydomonas monadinagroup) revised using an integrative approach

“…As shown in Fig. 1, we also confirmed that the psychrophilic strains isolated by Eddie et al (2008), Liu et al (2006) and Leya (2004) form a monophyletic lineage within Microglena, called the Polar-subclade.…”

“…Among Microglena species the pyrenoid is very variable in shape, but all strains have in common that the pyrenoid is surrounded by several or many starch grains arranged in parallel rows. This was also reported by Ettl & Green (1973) for M. reginae, by Rosowski & Hoshaw (1988) for M. longirubra, and Eddie et al (2008) and Liu et al (2006) for two unidentified psychrophilic Chlamydomonas strains, based on electron microscopical investigations. Pyrenoid shape varies according to morphotype (Fig.…”

“…This type, in which the chloroplast has a thick basal part, where the single large pyrenoid is located, is present in M. charkoviensis, M. reginae and M. uva-maris. Strains of the Polarsubclade were not the focus of our study, but comparisons with published pictures show that these strains also have a chloroplast of morphotype I (Leya, 2004;Liu et al, 2006;Eddie et al, 2008).…”

“…The phylogenetic analyses presented in Fig. 1 showed that all strains investigated in this study belonged to the Monadina-clade (¼Microglena; see below), together with several strains previously isolated and sequenced from snowfields or glaciers of polar regions or from marine habitats in Japan (the 'Polar-subclade' sensu Eddie et al, 2008, in Fig. 1).…”

“…As mentioned above, recent studies have shown that Chlamydomonas-like species isolated from snowfields and ice of different regions belong to the Monadina-clade (Leya, 2004;Liu et al, 2006;Eddie et al, 2008). We compared these data with our investigations of 15 strains previously designated as C. monadina from public culture collections and two marine species (C. reginae Ettl & J.C. Green and C. uva-maris Butcher), using the integrative approach proposed by Pro¨schold & Leliaert (2007).…”