Effect of Bacillus amyloliquefaciens and Bacillus subtilis on fermentation, dynamics of bacterial community and their functional shifts of whole-plant corn silage

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Effect of Bacillus amyloliquefaciens and

Bacillus subtilis on fermentation, dynamics

of bacterial community and their functional

shifts of whole-plant corn silage

Jie Bai

1,2

, Marcia Franco

, Zitong Ding

1,2

, Lin Hao

, Wencan Ke

1,2

, Musen Wang

1,2

, Dongmei Xie

1,2

, Ziqian Li

1,2

Yixin Zhang

1,2

, Lin Ai

and Xusheng Guo

1,2*

Abstract

Background: Bacillus amyloliquefaciens (BA) and Bacillus subtilis (BS) are usually used as feed supplements directly

or bacterial inoculants in biological feeds for animals. However, few research have reported the effects of BA and BS

on fermentation characteristics and bacterial community successions of whole-plant corn silage during ensiling. If

the BA and BS inoculants have positive effects on silages, then they could not only improve fermentation

characteristics, but also deliver BA or BS viable cells to ruminants, which would play its probiotic effect. Therefore,

the objectives of this study were to investigate the effects of BA and BS on the fermentation, chemical

characteristics, bacterial community and their metabolic pathway of whole-plant corn silage.

Results: Freshly chopped whole-plant corn was inoculated without or with BA and BS, respectively, and ensiled for

1, 3, 7, 14 and 60 d. Results showed that BA and BS inoculations increased lactic acid concentrations of whole-plant

corn silages compared with control, and BA inoculation decreased acetic acid concentrations, whereas BS

inoculation decreased fiber contents and increased crude protein (CP) content. Higher water-soluble carbohydrate

contents and lower starch contents were observed in BA- and BS-inoculated silages compared with that in control.

The decreased CP content and increased non-protein nitrogen content were observed in BA-inoculated silage,

which was consistent with the higher amino acid metabolism abundances observed in BA-inoculated silage. In

addition, it was noteworthy that BA and BS inoculations increased the metabolism of cofactors and vitamins, and

decreased the relative abundances of drug resistance: antimicrobial pathways. We also found that the bacterial

metabolism pathways were clearly separated into three clusters based on the ensiling times of whole-plant corn

silage in the present study. There were no significant differences in bacterial community compositions among the

three groups during ensiling. However, BA and BS inoculations decreased the relative abundances of undesirable

bacteria such as Acetobacter and Acinetobacter.

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* Correspondence: guoxsh07@lzu.edu.cn

State Key Laboratory of Grassland Agro-ecosystems, School of Life Sciences,

College of Pastoral Agriculture Science and Technology, Lanzhou University,

Lanzhou 730000, China

Probiotics and Biological Feed Research Centre, Lanzhou University,

Lanzhou 730000, China

Full list of author information is available at the end of the article

Bai et al. Journal of Animal Science and Biotechnology (2022) 13:7

https://doi.org/10.1186/s40104-021-00649-0

Conclusion: Our findings suggested that the BS strain was more suitable as silage inoculants than the BA strain in

whole-plant corn silage in this study.

Keywords: Bacillus silage inoculants, Function prediction, Silage quality, Zea mays

Introduction

Whole-plant corn silage, which makes up over 40% of

forage fed to dairy cows [1], has become the main

roughage used in ruminants’diet especially for dairy cat-

tle diets worldwide. Hence, nutrionally and hygiencially

high-quality silage is a crucial preprequisite for develop-

ing ruminant husbandary. To produce high quality sil-

age, silage inoculants are usually used to promote

fermentation process. In the report of Xu et al. [2], silage

inoculants were divided into four generations according

to their different functions during ensiling. Homolactic

bacteria, accelerating the lactic acid fermentation and

improving the fermentation quality and nutrients preser-

vation of silage, were identified as the first generation in-

oculants. Heterolactic bacteria, improving aerobic

stability by producing acetic acid and 1, 2-propanediol,

were subsequently identified as second generation inocu-

lants. Some strains with special functions, such as feru-

loyl esterases-producing Lactobacillus plantarum [3]or

Pediococcus acidilactici with high-antioxidant activity [4]

that improved the digestibility of fiber or antioxidant

capacity in silages, were defined as third generation inoc-

ulants. Directly fed microbes, such as Saccharomyces cer-

evisiae, were defined as fourth generation silage

inoculants where probiotic microbes delivered direct

benefits to the animals through silages. Bacillus could

also be classified as fourth generation silage inoculants

because of its favorable ability to improve animal per-

formance when orally administered [5] and improve fer-

mentation quality and aerobic stability in alfalfa silages

[6].

Bacillus amyloliquefaciens and Bacillus subtilis are

usually used as biological control agents to protect

plants effectively against plant pathogens [7,8]. In

addition, due to the antimicrobial ability of B. amyloli-

quefaciens and B. subtilis, they are used as feed supple-

ments directly or bacterial inoculants in biological feeds

for monogastric animals, such as poultry and pigs [9–

11]. There are also some studies reported the application

of B. subtilis in silages. Lara et al. [12] and Bai et al. [6]

found that B. subtilis used in silages improved fermenta-

tion quality and inhibited aerobic spoilage. However, few

research have reported the effects of B. amyloliquefa-

ciens on fermentation characteristics in silages. Sansine-

nea and Ortiz [13] reported that B. amyloliquefaciens

was related to B. subtilis and had the potential to pro-

duce many antimicrobial compounds. Thus, we specu-

lated that B. amyloliquefaciens could also improve

fermentation characteristics of silages and deliver B.

amyloliquefaciens viable cells to ruminants.

Understanding the succession of bacterial community

could provide deep insight into the fermentation process

underlying silage formation. The bacterial community

succession at different phases of ensiling is a dynamic

process that varies throughout the fermentation period,

and single-molecule real-time (SMRT) sequencing tech-

nologies provide useful information on microbial shifts

at the species level [14]. In addition, the potential func-

tions of bacterial communities were predicted in some

studies, such as Zhang et al. [15] and Bai et al. [16],

where they found that the main bacterial functions could

explain the material conversion during the composting

or ensiling process. To date, the effects of lactic acid

bacteria (LAB) inoculants on bacterial community diver-

sity and succession of silages using SMRT sequencing

technology have been evaluated in previous studies [16,

17]. LAB, as a commonly used silage inoculants, have

been studied a lot in alfalfa silages. However, few re-

searches have reported the effects of B. amyloliquefa-

ciens or B. subtilis on bacterial community succession

and their functional shifts in whole-plant corn silage.

Therefore, the objective of this study was to investigate

the effects of B. amyloliquefaciens or B. subtilis on the

fermentation characteristics, bacterial community suc-

cession and their functional shifts of whole-plant corn

silage during ensiling.

Materials and methods

Silage preparation

Whole-plant corn (Zea mays L. Dajingjiu 3876) was har-

vested at half milk-line from 4 randomly selected sites in

a commercial farm located in Dingxi city, Gansu prov-

ince, China. The whole-plant corn was chopped into 2

cm size by using a forage cuter (Toyohira Agriculture

Machinery, Sapporo, Japan) and then taken into the la-

boratory immediately. For each of the 4 randomly se-

lected sites, there were 15 piles of forage (1 untreated

pile and 2 inoculated piles for each fermentation time of

1, 3, 7, 14 and 60 d). The corn forage piles were treated

separately with distilled water (control, CK); Bacillus

amyloliquefaciens HRH

317

(BA, 1 × 10

colony-forming

unit/g fresh matter, provided by Shanxi Agricultural

University, China), which could inhibit fungus by produ-

cing antifungal proteins [18]; Bacillus subtilis CP7 (BS,

1×10

colony-forming unit/g fresh matter, provided by

Zhangye Aolin Beier Biological Technology Co., Ltd.,

Bai et al. Journal of Animal Science and Biotechnology (2022) 13:7 Page 2 of 14

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Effect of Bacillus amyloliquefaciens and Bacillus subtilis on fermentation, dynamics of bacterial community and their functional shifts of whole-plant corn silage

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