Elsevier

Rhizosphere

Volume 18, June 2021, 100350
Rhizosphere

Exposure to elevated nutrient load results in structural and functional changes to microbial communities associated with riparian wetland plants Phalaris arundinaceae and Veronica anagallis-aquatica

https://doi.org/10.1016/j.rhisph.2021.100350Get rights and content

Abstract

The goal of this study was to better understand the resilience of rhizosphere microbial communities located in riparian wetlands subjected to high nutrient loads following effluent or runoff exposure. Specifically, this research monitored functional profiles of mesocosm communities during an artificial high nitrogen load exposure following adaptation to high or low water quality conditions. Based on prior research, two species of wetland plants were chosen, Phalaris arundinaceae and Veronica anagallis-aquatica, both located in local riparian zones, and planted in wetland mesocosms. Rhizosphere bacterial community response was monitored for approximately three weeks after exposure to elevated nutrient loads, following prior adaptation for several months to either high or low (poor) water quality conditions. The impact of prior acclimation conditions was then assessed. Changes to rhizosphere bacterial community structure and function were monitored using PCR-denaturing gel gradient electrophoresis (DGGE) and Biolog™ Ecoplates, respectively. Plants were also sampled to assess any impact on mycorrhizal associations over the exposure period. As an additional indicator of functionality and nitrogen utilization within the mesocosm system, inorganic intermediate N species were monitored at the outflow. Significant differences were observed over time following elevated nutrient exposure in bacterial structural diversity and richness, as well as functional diversity and richness (p < 0.001). The effects of interactions between time, plant species and water quality exposure were also significant for both structural (p = 0.002) and functional (p = 0.05) community diversity. Elevated nutrient exposure resulted in changes to microbial carbon source utilization profiles, specifically, bacterial usage of amino acids (p = 0.032), polymers (p = 0.029) and carboxylic and ketonic acids (p = 0.042). Carboxylic and ketonic acid utilization by bacterial communities was positively correlated with the removal of nitrate and nitrite from experimental mesocosms. Mycorrhizal associations as measured by percent colonization also decreased significantly in P. arundinaceae following elevated nutrient exposure (p < 0.001). Furthermore, abundance of nitrogenous compounds in outflow water differed between plant species treatments, with V. anagallis-aquatica removing more nitrate from the outflow (p = 0.005) while P. arundinaceae removed higher levels of ammonia (p = 0.03). This study provides insight into how microbial communities respond to transient nutrient loads such as that experienced by overland runoff following a high rain event and will assist in the design and rehabilitation of wetlands or riparian buffer strips to manage higher nutrient loads resulting from increasing human activity impacting our freshwater systems.

Introduction

Anthropogenic activities are increasingly impacting our freshwater ecosystems (Mekonnen and Hoekstra, 2015). Nitrogen and phosphorous are among the most common nutrients entering aquatic ecosystems in excess and can have detrimental effects on ecosystem dynamics and the health of aquatic plants and animals (Lamers et al., 2002; Wang et al., 2007; Faulwetter et al., 2009). Water quality in aquatic freshwater systems is of serious concern as eutrophication resulting from human activities has already been attributed to losses in biodiversity (Tilman et al., 2001; Hautier et al., 2009; Hooper et al., 2012). The usefulness of wetland areas in the remediation of high nutrient water is increasingly prevalent in the literature and in practice (Hua et al., 2017; Wu et al., 2014; Vymazal et al., 2013; Bialowiec et al., 2011; Huang et al., 2000). Nitrogen plays an important role in the biogeochemical cycle of natural wetlands and its primary mechanism of removal from impacted waters occurs via biological pathways, which are microbial in nature, including ammonification, nitrification, denitrification, ammonium oxidation, and microbial assimilation (Kadlec and Wallace 2008; Vymazal and Kropfelova 2008; Humbert et al., 2012).

The presence of plants plays an important role in shaping the microbial community in natural and treatment wetlands and has a primarily positive influence on the removal of inorganic sources of nitrogen (Vymazal, 2011). The rhizosphere, the area around plant roots actively influenced by the physiological activities occurring in the plant, plays an important role in contaminant removal. This is because the rhizosphere, including roots, bacterial communities and mycorrhizal fungi, establish environmental conditions conducive to the removal of many contaminants including inorganic nutrients. The plant roots supply oxygen to the rhizosphere which promotes aerobic microbial metabolism and, also, creates an oxygen gradient which allows for micro-environments favoring both aerobic and anaerobic microbial processes, as well as those which occur at the aerobic-anaerobic interface (Schulz et al., 2003). The production of oxygen by plant roots is variable among plant species, as such the efficiency of oxygen-dependent microbial processes is likely to also be plant-species dependent (Lai et al., 2011; Peng et al., 2014).

It is important to understand how microbial communities may be affected by changes in water quality within wetlands to better understand how increasing anthropogenic impacts may affect the ecosystem services they provide. Some of the methods we can use to assess changes in microbial communities are based on examination of changes to community structural characteristics, such as bacterial diversity and richness, and by monitoring changes to community function. Community function can be assessed by a variety of different methods such as monitoring microbial enzyme activity and the degradation of various relevant substrates (e.g. Zak et al., 1994; Kourtev et al., 2002; Menon et al., 2013; Clairmont and Slawson, 2019). Biolog™ EcoPlates present a unique method of assessing community functional shifts by looking at the utilization of 31 different carbon sources by whole microbial communities (Garland and Mills, 1991; Zak et al., 1994; Weber and Legge, 2009). They have been employed to assess functional community changes within a variety of different habitat types over a wide range of different environmental conditions (e.g. Insam, 1997; Weber et al., 2008; Floch et al., 2011). Very few studies have investigated how water quality, particularly, nutrient pollution, affect microbial communities within wetland ecosystems (e.g. Ravit et al., 2003; Mentzer et al., 2006; Ahn et al., 2007; Cao et al., 2008; Helt et al., 2012). Of these studies, only a handful examines this question within naturally-occurring wetland systems (e.g. Ravit et al., 2003; Cao et al., 2008). The findings from these studies have been mixed, with some studies indicating that nutrient pollution does impact microbial community structure and/or function (Ravit et al., 2003; Mentzer et al., 2006; Ahn et al., 2007; Clairmont and Slawson, 2020; Clairmont et al., 2020), while others have found no noticeable difference between impacted and unimpacted communities (e.g. Cao et al., 2008). Clearly, more investigation is needed into this matter to better understand how increasing anthropogenic impacts are affecting the resilience of microbial communities in natural wetland systems.

The objective of this study was to examine the effects of two different parameters (plant species and previous water quality treatment exposure) on wetland rhizosphere bacterial communities and their ability to remediate water impacted with high nitrogen levels. The study design aimed to simulate a riparian zone, or buffer strip wetland area receiving high nutrient-impacted water from a non-point source such as runoff during high rain events. We hypothesized that microbial communities previously adapted to different water quality conditions (high vs low) and different plant species associations would differ in their response and ability to accommodate the increased nutrient load.

Section snippets

Mesocosm set up and design

Twelve wetland mesocosms simulating riparian conditions were constructed from 90.92 L glass aquariums (610 mm Length x 406 mm Height x 305 mm Width) (Marineland, Virginia, USA). A peristaltic pump was used to distribute water in a drop-wise fashion to each mesocosm from the top (Masterflex 12 channel peristaltic pump with 2.76 mm santoprene tubing, Cole Parmer, Quebec, CA), and the tanks subsequently filled through natural adsorptive processes of the soil media. Pea gravel (King, Ontario, CA)

Removal of inorganic nutrients from high nutrient water

There were no differences between the high and low water quality exposures in the release of inorganic nitrogen or phosphorus by the experimental mesocosms (Table 1). However, plant species differences in the release of nitrate from the mesocosms were observed (p = 0.005) between P. arundinaceae and V. anagallis-aquatica, with V. anagallis-aquatica releasing significantly less nitrate following exposure to the high nutrient water. Conversely, P. arundinaceae released significantly less ammonia

Discussion

In response to our hypothesis that different plant species and the type of prior water quality exposure would result in different abilities of wetland rhizosphere communities to accommodate nutrient loads, we found that water quality type (high vs low) during prior exposure resulted in differences related to plant species that were significant as reflected by the release of both nitrate and ammonia from the high nutrient impacted water. Interestingly, P. arundinaceae establishment resulted in

Conclusions

Plant species significantly influenced the ability of mesocosms to remediate nutrient loads. Specifically, P. arundinaceae performed better at the removal of ammonia while V. anagallis-aquatica was more efficient in the removal of nitrate. The association of particular plant species with more efficient removal of a particular inorganic nutrient can guide plant species selection for riparian zone rehabilitation and wetlandestablishment. Both plant species and exposure to previous water quality

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) Ottawa, ON [GR-RGPGP 2014-00060-R]; the Ontario Water Consortium (OWC) Waterloo, ON.

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