A Bacterial Pathogen Displaying Temperature-Enhanced Virulence of the Microalga Emiliania huxleyi

Abstract

Emiliania huxleyi is a globally abundant microalga that plays a significant role in biogeochemical cycles. Over the next century, sea surface temperatures are predicted to increase drastically, which will likely have significant effects on the survival and ecology of E. huxleyi. In a warming ocean, this microalga may become increasingly vulnerable to pathogens, particularly those with temperature-dependent virulence. Ruegeria is a genus of Rhodobacteraceae whose population size tracks that of E. huxleyi throughout the alga’s bloom–bust lifecycle. A representative of this genus, Ruegeria sp. R11, is known to cause bleaching disease in a red macroalga at elevated temperatures. To investigate if the pathogenicity of R11 extends to microalgae, it was co-cultured with several cell types of E. huxleyi near the alga’s optimum (18°C), and at an elevated temperature (25°C) known to induce virulence in R11. The algal populations were monitored using flow cytometry and pulse-amplitude modulated fluorometry. Cultures of algae without bacteria remained healthy at 18°C, but lower cell counts in control cultures at 25°C indicated some stress at the elevated temperature. Both the C (coccolith-bearing) and S (scale-bearing swarming) cell types of E. huxleyi experienced a rapid decline resulting in apparent death when co-cultured with R11 at 25°C, but had no effect on N (naked) cell type at either temperature. R11 had no initial negative impact on C and S type E. huxleyi population size or health at 18°C, but caused death in older co-cultures. This differential effect of R11 on its host at 18 and 25°C suggest it is a temperature-enhanced opportunistic pathogen of E. huxleyi. We also detected caspase-like activity in dying C type cells co-cultured with R11, which suggests that programmed cell death plays a role in the death of E. huxleyi triggered by R11 – a mechanism induced by viruses (EhVs) and implicated in E. huxleyi bloom collapse. Given that E. huxleyi has recently been shown to have acquired resistance against EhVs at elevated temperature, bacterial pathogens with temperature-dependent virulence, such as R11, may become much more important in the ecology of E. huxleyi in a warming climate.

Recognition cascade and metabolite transfer in a marine bacteria‐phytoplankton model system

“…An improved understanding of bacteria-phytoplankton interactions will require knowledge of the molecules exchanged between the cells and information on whether or not specific recognition mechanisms play a role. The configuration of such interactions is likely to be extremely diverse, since examples of bacteria-phytoplankton relationships vary broadly from pathogenic to mutualistic (Mayali and Azam, 2004;Seyedsayamdost et al, 2011;Xie et al, 2013;Amin et al, 2015;Aharonovich and Sher, 2016;Mayers et al, 2016;Segev et al, 2016). Most direct interactions are proposed to take place in the phycosphere, a diffusive boundary layer immediately surrounding phytoplankton cells that is enriched in organic matter (Bell and Mitchell, 1972).…”

Coccolithoviruses: A Review of Cross-Kingdom Genomic Thievery and Metabolic Thuggery

“…Bacteria are important constituents of microbial food webs in marine habitats [50,51] and may themselves act as pathogens. As an example of the latter, certain bacteria have been found to induce caspase-like activity and cell death in E. huxleyi [52]. Diseases of macroalgae in coastal habitats have also been attributed to bacteria [53], which likely coexist with a diverse viral community [54].…”

The Bacterial Symbiont Phaeobacter inhibens Shapes the Life History of Its Algal Host Emiliania huxleyi

“…This resistance of N-type cells to pathogenic roseobacters has been previously reported for the N-type strain, CCMP2090, cultured with Ruegeria sp. R11 (Mayers et al, 2016). Together, these findings suggest that, although the N cell used in the current study (CCMP2090) was recently derived from a polymicrobial calcifying parent strain (CCMP1516), calcifying and noncalcifying diploid strains have important biological differences, which might for instance confer widespread resistance to roseobacter pathogenesis.…”

“…Similarly, the closely related roseobacter pathogen, Ruegeria sp. R11 (Fernandes et al, 2011) (also known as Nautella italica R11; Vandecandelaere et al, 2009;Rodrigo-Torres et al, 2016), kills C and S cells and not N cells (Mayers et al, 2016). While the mechanism of P. inhibens pathogensis is not known, clues can be found in EhVs, which upregulate metacaspase activity in calcifying diploid cells, inducing alga PCD (Bidle et al, 2007).…”

“…The activation of algal caspase-like molecules resulting in apoptosis-like PCD has already been described in the pathogenic interaction between Ruegeria sp. R11 and the C-and S-type culture CCMP3266 (Mayers et al, 2016).…”