Aluminum and acidity suppress microbial activity and biomass in acidic forest soils

https://doi.org/10.1016/j.soilbio.2016.02.019Get rights and content

Highlights

  • Soluble and exchangeable Al levels were elevated in acidic forest soils.

  • Exchangeable Ca and Mg concentrations were lowered in acidic forest soils.

  • Enzyme activities associated with C, N, and P cycling were suppressed by Al toxicity.

  • By binding to organic matter, Al and Fe limit microbial biomass in Andisols.

Abstract

To evaluate the effects of aluminum (Al) toxicity on microbial processes in acidic forest soils, we determined microbial biomass, soil enzyme activities associated with carbon (C), nitrogen, and phosphorus cycling (β-d-glucosidase and polyphenol oxidase, l-asparaginase, and acid phosphatase, respectively), exchangeable base cations, soluble and exchangeable Al (CaCl2–Al and KCl–Al), and organically bound (Alp and Fep) and both organically bound and noncrystalline forms (Alo and Feo) of Al and iron (Fe) in Japanese forest soils (25 Inceptisols, seven allophanic Andisols, and eight nonallophanic Andisols). The exchangeable calcium (Ca) and magnesium (Mg) concentrations decreased significantly with decreasing soil pH. In contrast, the KCl–Al and CaCl2–Al concentrations exponentially increased with decreasing pH, and the increase was steeper in Andisols than in Inceptisols. The Alp concentration also increased exponentially with decreasing soil pH in Andisols, and the Fep concentration increased in Andisols and Inceptisols, whereas the concentration of the noncrystalline Al pool (Alo − Alp) decreased with decreasing pH in Andisols. We showed that the β-d-glucosidase, polyphenol oxidase, and acid phosphatase activities were mainly suppressed by soluble and exchangeable Al, whereas l-asparaginase activity was depressed by soil pH. In Andisols, a negative effect of organically bound Al and Fe on the biomass C/organic C ratio was observed. These results suggest that Al toxicity and acidity repressed soil enzyme activities, leading to suppressed microbially mediated nutrient cycling, and that Al toxicity and a reduced availability of organic matter, as a result of Al and Fe binding, may protect a substantial pool of organic C from microbial degradation in acidic forest soils.

Introduction

Acidity develops naturally in soils of relatively humid areas, including Japan, and acidic soils with pH < 5.5 account for approximately 30% of the world's ice-free land area (Hodson and Donner, 2013). Acidification in forest soils is accelerated by acid deposition from anthropogenic sources. In North America and Europe, acid deposition damaged forest and aquatic ecosystems during the later decades of the 20th century (Miller, 2002). Growth-limiting factors for plants in acidic soils include aluminum (Al) and hydrogen (H) toxicities, as well as deficiencies of essential elements such as calcium (Ca) and magnesium (Mg) (Foy, 1984); Al toxicity is considered to be one of the most deleterious factors for plant growth in acidic soils. According to Foy (1984), Al toxicity is more important than toxicity related to pH in limiting the growth of higher plants in many acidic soils (pH > 4.0).

Because of efforts to reduce sulfur (S) and nitrogen (N) emissions starting in the mid-to-late 20th century, acid deposition has been largely reduced in North America and Europe (Lajtha and Jones, 2013), although there are still widespread areas of ongoing acidification in forest soils in the United States (Greaver et al., 2012). In stark contrast, rates of S deposition and N deposition have recently increased in Japan: the annual increase rate was 1.69% y−1 for non-seasalt SO42− wet deposition during 1981–2005 (Kuribayashi et al., 2012) and ∼4% y−1 for NO3 wet deposition during 1994–2008 (Morino et al., 2011). The average pH of precipitation from 2003 to 2007 was 4.68 in Japan, and strong acidic precipitation (pH < 4.0) accounted for 4.5% of the total precipitation at 14 sites where daily sampling has been conducted (Ministry of the Environment, 2009). Transboundary pollution has largely accounted for the increased acid deposition in Japan. China was estimated to account for 34% of the S deposition from 1981 to 1985 and 51% from 2001 to 2005 (Kuribayashi et al., 2012), while it accounted for 29–35% of the NO3 wet deposition from 1989 to 1993 and 43–61% from 2004 to 2008 (Morino et al., 2011) in Japan. Although no apparent impacts of acid deposition on ecosystems have been observed in Japan, in the future, negative impacts might occur if the acid deposition rate remains at its current level (Ministry of the Environment, 2006).

Al toxicity to plants, especially crops, has been studied extensively (Matsumoto, 2000). In contrast, although many studies have addressed the effects of acid deposition on soil microorganisms, most of the studies have only examined the effects of increased acidity (Wolters and Schaefer, 1994), and little information exists regarding the impact of elevated levels of soluble and exchangeable Al on soil microbial processes in forest soils (e.g., Illmer et al., 1995, Kanazawa and Kunito, 1996, Joner et al., 2005). In almost all forest ecosystems with acidic soils, woody plants do not show apparent stress symptoms in response to Al toxicity (Brunner and Sperisen, 2013), but soil microorganisms and microbially mediated nutrient cycling might be affected by Al toxicity. Kraal et al. (2009) reported that the addition of Al suppressed soil respiration, nitrification, and the microbial uptake of NH4+ in pine litter. Additionally, the diversity of Al-resistant microorganisms, which are likely to play a key role in various microbially mediated processes in acidic forest soils, is low (Kunito et al., 2012a), which might result in their low functional diversity. In the present study, we investigated the effects of Al on microbial biomass and soil enzyme activities associated with carbon (C), N, and phosphorus (P) cycling in Japanese forest soils. In addition to toxicity of soluble and exchangeable Al, noncrystalline and organically bound forms of Al might limit microbial activity, because they have been reported to stabilize organic matter (Baldock and Skjemstad, 2000, Kleber et al., 2015). Hence, these Al and Fe pools, as well as soluble and exchangeable Al, were determined.

Section snippets

Soils

Soil samples were collected by hand trowel from a 0–15-cm depth in the A horizon of forest soils in Nagano Prefecture, Japan: 25 soils were classified as Inceptisols (Brown Forest soils in the Japanese system), seven soils were classified as allophanic Andisols (Allophanic Kuroboku soils in the Japanese system), and eight soils were classified as nonallophanic Andisols (Nonallophanic Kuroboku soils in the Japanese system). Sampling sites were located at elevations ranging from 480 m to 2050 m

Results

All of the chemical and microbial properties of the soils, other than the organically bound and noncrystalline forms of Al and Fe, did not significantly differ among the soil types (Table 1, Table 2). The highest levels of Alp, Fep, and Feo were found in the nonallophanic Andisols, and the lowest levels were found in the Inceptisols. The allophanic Andisols showed the highest concentrations of Alo, and the highest Alo − Alp and Feo − Fep values. There was a strong positive correlation between

Discussion

In acidic forest soils in Japan, soluble and exchangeable Al levels increased with declining pH, whereas exchangeable Ca and Mg concentrations declined with reduction of pH (Fig. 1). It has been widely recognized that soil acidification leads to elevated concentrations of soluble and exchangeable Al and to decreased concentrations of exchangeable Ca and Mg (e.g., Bailey et al., 2005). Saigusa et al. (1980) noted that a slight Al-mediated injury was observed in the roots of an Al-sensitive plant

Conclusions

Soluble and exchangeable Al levels were increased with a fall in pH, whereas exchangeable Ca and Mg levels were lowered with falling pH in acidic forest soils in Japan. High soil acidity increased the KCl–Al and CaCl2–Al levels to a greater degree in the Andisols than in the Inceptisols. Forest ecosystems comprising nonallophanic Andisols seem to be especially susceptible to acidity, as the low availability of Ca and Mg, as well as the high level of soluble and exchangeable Al, can be expected

Acknowledgment

This study was supported by a Grant-in-Aid for Young Scientists (B) (No. 16710002) from the Ministry of Education, Culture, Sports, Science and Technology, Japan.

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