Responses of a Bacterial Pathogen to Phosphorus Limitation of Its Aquatic Invertebrate Host

Abstract

Abstract. Host nutrition is thought to affect the establishment, persistence, and severity of pathogenic infections. Nutrient-deficient foods possibly benefit pathogens by constraining host immune function or benefit hosts by limiting parasite growth and reproduction. However, the effects of poor elemental food quality on a host's susceptibility to infection and disease have received little study. Here we show that the bacterial microparasite Pasteuria ramosa is affected by the elemental nutrition of its aquatic invertebrate host, Daphnia magna. We found that high food carbon : phosphorus (C:P) ratios significantly reduced infection rates of Pasteuria in Daphnia and led to lower within-host pathogen multiplication. In addition, greater virulent effects of bacterial infection on host reproduction were found in Daphniaconsuming P-deficient food. Poor Daphnia elemental nutrition thus reduced the growth and reproduction of its bacterial parasite, Pasteuria. The effects of poor host nutrition on the pathogen were further evidenced by Pasteuria's greater inhibition of reproduction in P-limited Daphnia. Our results provide strong evidence that elemental food quality can significantly influence the incidence and intensity of infectious disease in invertebrate hosts.

Synergistic effects of dual parasitism in Daphnia magna under nutrient limitation

“…These food quality treatments were not chosen to mimic the natural environment of the Daphnia individuals, but rather to generate a gradient ranging from low to extreme food limitation. By manipulating the absolute N content rather than decreasing P in the medium, we aimed to induce severe food limitation in the Daphnia (rather than solely implementing P-limitation), as both a high absolute N-concentration and high N:P ratio have been shown to be detrimental for Daphnia (frost et al 2008;DaLLas & DraKe 2014). For each S. obliquus culture, we measured the algal C, N and P-content.…”

“…The outcome of the interaction between host and parasite depends on the amount of energy available for the host, the allocation of this energy towards life history responses, and the need and capacity of the parasite to exploit this (smith & hoLt 1996;BeDhomme et al 2004;PeDerson & fenton 2007;miDeo 2009;cressLer et al 2014). In general, parasite virulence is expected to increase upon nutrient limitation of the host, due to increased resource competition between both antagonists (ferguson & reaD 2002;LamBrechts et al 2006;frost et al 2008;cornet et al 2014). Resource availability will also affect (especially costly) host immune defenses (oJaLa et al 2005;KaPari et al 2006;KLemoLa et al 2007;LittLe & KiLLicK 2007), especially if there is a metabolic link between their resources, given that host immunity and parasites then interact as "competitors" (cressLer et al 2014).…”

“…A shortage of energy and elements impacts the interaction of Daphnia with its parasites (frost et al 2008;haLL et al 2009;DaLLas & DraKe 2014;aaLto et al 2015;DecaestecKer et al 2015). In natural systems, parasitism of Daphnia individuals is the rule rather than the exception, with multiple infections occurring frequently (DecaestecKer et al 2005;eBert 2005;woLinsKa et al 2009;Jansen et al 2010;Lange et al 2014).…”

“…In natural systems, parasitism of Daphnia individuals is the rule rather than the exception, with multiple infections occurring frequently (DecaestecKer et al 2005;eBert 2005;woLinsKa et al 2009;Jansen et al 2010;Lange et al 2014). Because of their tight association, parasites can compete for nutrients with their host (frost et al 2008;haLL et al 2009). We here investigate how severe food deprivation impacts the virulence of single versus multiple parasite exposure in Daphnia magna (Straus, 1820).…”

No uniform associations between parasite prevalence and environmental nutrients

“…Parasites, in turn, are capable of shaping host population dynamics (Hudson et al 1998, Johnson et al 2009, Hall et al 2011, through modifying life-history traits of host individuals. However, recent experimental evidence suggests that in addition to host availability, nutritional status and especially the stoichiometric quality (i.e., carbon-nitrogen-phosphorus ratio [C:N:P] of the host) are connected to parasite transmission success, production of infective propagules within the host, and parasite virulence (Pulkkinen and Ebert 2004, Frost et al 2008a, b, Hall et al 2009, Seppa¨la¨et al 2011). Host population dynamics and nutritional status, in turn, are altered by environmental conditions.…”